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Molecular insights into probiotic mechanisms of action employed against intestinal pathogenic bacteria

Winschau F. van Zyl, Shelly M. Deane, Leon M.T. Dicks

Gut Microbes · 2020 · Review

doi:10.1080/19490976.2020.1831339

Abstract

Gastrointestinal (GI) diseases, and in particular those caused by bacterial infections, are a major cause of morbidity and mortality worldwide. Treatment is becoming increasingly difficult due to the increase in number of species that have developed resistance to antibiotics. Probiotic lactic acid bacteria (LAB) have considerable potential as alternatives to antibiotics, both in prophylactic and therapeutic applications. Several studies have documented a reduction, or prevention, of GI diseases by probiotic bacteria. Since the activities of probiotic bacteria are closely linked with conditions in the host's GI-tract (GIT) and changes in the population of enteric microorganisms, a deeper understanding of gut-microbial interactions is required in the selection of the most suitable probiotic. This necessitates a deeper understanding of the molecular capabilities of probiotic bacteria. In this review, we explore how probiotic microorganisms interact with enteric pathogens in the GIT. The significance of probiotic colonization and persistence in the GIT is also addressed.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 19, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

Lactic acid bacteria (LAB) play a major role in the preservation and organoleptic profile of fermented food products, but are equally important in affecting the composition and diversity of intestinal microbiota. Some of the most important beneficial effects include stimulation of the host’s immune system, prevention of antibiotic-associated diarrhea, treatment of inflammatory bowel disease (IBD) and irritable bowel syndrome (IBS), alleviation of lactose intolerance, lowering of cholesterol levels and prevention of life-threatening GI infections such as Clostridium difficile-associated diarrhea. Renewed interest in probiotics initiated the launch of an increasing number of probiotic-containing supplements that claim to confer specific health benefits to the consumer., Many of these products are driven by aggressive marketing through pharmaceutical and nutritional companies, often without a clear understanding of the interactions between probiotic bacteria, normal commensal microorganisms, pathogens and the host.

Lactic acid bacteria are indigenous to the small and large intestine of humans and animals and exert a number of probiotic properties, such as binding to receptors and physically excluding pathogens, production of antimicrobial substances, strengthening of the gut mucosal barrier and modulation of the immune system. It is therefore important to have an in-depth understanding of the specific metabolic and genetic interactions between probiotic bacteria, the host intestinal mucosa and enteric pathogens in the GIT. Commensal bacteria also act as a protective barrier against pathogens by providing mucosal protection and stimulation of the immune system., The most predominant genera used in probiotic supplements are Lactococcus, Lactobacillus and Bifidobacterium spp. derived from humans and animals. It is important that probiotic strains survive passage through the stomach, resist bile salts and digestive enzymes in the small intestinal tract and reach the colon in sufficient numbers. The number of viable cells surviving the journey through the GIT is, however, strain specific and depends on the dosage and duration of administration.,

Due to the complex nature of the human GIT, only a few in-depth studies on interactions between probiotic bacteria and enteric pathogens have been published and many rely on in vitro data to decipher the mechanistic basis underlying a specific health benefit. A specific health benefit may also be attributed to a combination of mechanisms. This is important, as strains from the same species may evoke different responses in the host. Several probiotic strains secrete secondary metabolites and peptides with antimicrobial activity that may interact directly with the host or pathogens., Ultimately, a detailed characterization of these interactions will significantly improve the application of probiotics to support and enhance human health. In this review, the mechanisms probiotic bacteria use to interact with enteric pathogens, and the ability to colonize the GIT, are discussed.

Colonization and persistence of probiotic bacteria in the GIT

Strains that colonize the GIT have a greater beneficial effect on the host than strains passing through the GIT. This may be because adhesion to mucus and epithelial cells not only provides the strain with a competitive advantage, but forms a stronger interaction with the host that leads to recognition of the probiotic and stimulation of the host’s immune response., Furthermore, colonization by probiotic strains prevents adhesion of enteric pathogens to intestinal cells. Several studies have shown how probiotics interfere with the ability of GI pathogens, such as Salmonella typhimurium, Clostridium sporogenes and Enterococcus faecalis, to adhere to Caco-2 cells. A diverse spectrum of pathogens targeted by probiotic bacteria and their reported health promoting effects is listed in Table 1.

Earlier studies on the colonization of probiotics were based on in vitro studies demonstrating the ability of strains to adhere to cell lines such as Caco-2, HT-29 and HT29-MTX., Although these studies simulated GIT-models and have provided valuable insights into the adherence of probiotic cells, it remains an in vitro approach that is unable to recapitulate the complex multicellular nature of the GIT. Studies using cell lines require specialized equipment and facilities to keep the cells viable. Because of these reasons, studies on the survival and colonization of probiotic bacteria are mostly done by analyzing fecal samples. From the recovery of cells in feces after probiotic intervention, the persistence of strains is calculated, providing that cell numbers in the dosage are known and all methods are standardized. Probiotic cells that persist in feces for the longest time and highest numbers indicate a higher colonization and persistence in the GIT. In vivo pharmacokinetics of probiotics can be studied by comparing cell numbers (in fecal material) between specific strains before and after ingestion., Other techniques used include intestinal intubation and pyxigraphy. Antibiotic resistance markers can be used to clearly identify probiotic cells in fecal samples., When no strain identification is used, results may be difficult to interpret, since endogenous probiotic cells can also be excreted in feces. The pharmacokinetics of different probiotic LAB using fecal recuperation are listed in Table 2. The survival and persistence of ingested probiotics differs greatly between genera and even between strains. Lactobacillus and Bifidobacterium spp. have been extensively explored as probiotics, since they form an integral part of the natural gut microbiome of humans and animals., Bifidobacterium lactis LAFTI B94, B. longum SB T2928, Lactobacillus rhamnosus DR20, Lactobacillus gasseri SBT2055 and Enterococcus mundtii ST4SA persisted in high numbers for the longest time Table 2. In comparison, fecal recuperation of Lactococcus lactis MG 1363 and Lactobacillus fermentum KLD was much lower. In a recent study, the probiotic strains Lactobacillus plantarum 423 and E. mundtii ST4SA were transformed with a plasmid containing the bioluminescence firefly luciferase gene (ffluc) from Photinus pyralis. This allowed monitoring of the migration of the strains through the GIT and in mouse feces in real time and in a noninvasive manner. With the use of bioluminescent imaging (BLI), the authors detected cell numbers as low as 104 CFU/100 mg feces. Imaging revealed that E. mundtii ST4SA persisted in feces throughout the trial period (>20 days), whilst L. plantarum 423 persisted for 13 days after the last day (day 5) of intragastric administration. BLI provides three-dimensional images of cells as they migrate through the GIT (65). Information is gathered in real-time, using an in vivo imaging system (IVIS). Only metabolically active cells are detected. The technique has been used in several studies.,,,, Van Zyl et al. used BLI to study the transit of L. plantarum 423 and E. mundtii ST4SA in the digestive tract of mice for 9 consecutive days. Data generated using the technique correlated with viable cell counts. For a review on the application of optical imaging systems in in vivo tracking of LAB, the reader is referred to ref. 66.

Some reports have suggested that non-viable and non-colonizing probiotics may also confer certain health benefits to the host.,, During GI passage, non-colonizing, or transiently colonizing probiotic bacteria continue to be metabolically active, thus conferring beneficial health effects to their host. In a study by Kullen et al. human volunteers were administered a probiotic strain of Bifidobacterium and the recovery of the strain in feces was monitored. The strain was detected in feces at increasing cell numbers during days (8 days) of administration, but could not be recovered in fecal material after the last oral administration. The authors concluded that although the administered strain did not colonize the human GIT, colonization and prolonged persistence may not be required to achieve a significant probiotic effect. Similar results were reported by Fujiwara and coworkers., The authors found that bifidobacteria produce a 100 kDa protein, which actively prevents the adherence of pathogenic Escherichia coli to intestinal mucosal cells by blocking their binding to the glycolipid binding receptor gangliotetraosylceramide. Therefore, the competitive exclusion of the pathogenic strain may not have been related to direct live cell-to-cell competition for intestinal adhesion sites.

Microorganisms found in fecal samples are usually inhabitants of the lower intestine, such as the colon. In humans, intubation at specific intestinal sites is used to determine probiotic colonization in the upper sections of the GIT. Biopsies can be taken of the portions of the intestinal tract where probiotics are likely to colonize, proliferate and produce their metabolites.,,, Lactobacillus rhamnosus GG is one of the best studied probiotic strains and plays a role in the prevention or treatment of antibiotic-associated diarrhea, flatulence, rotavirus gastro-enteritis, and stomach and abdominal pain.,,, However, when L. rhamnosus GG in fermented milk was administered to human volunteers, the strain showed only limited persistence in feces and could not be recovered in 67% of the subjects after 7 days of the last dosage. The same results were obtained when a milk formula containing the strain was fed to premature infants. However, Alander et al. did recover L. rhamnosus GG from colonic biopsies for lengthy periods after administration ceased. Human volunteers were administered with 6 × 1010 CFU of L. rhamnosus GG twice a day for 12 consecutive days. Cell numbers of L. rhamnosus GG in the feces decreased with time after the last bacterial dosage was administered. No cells of strain GG were detected in feces 14 days after the last dosage. However, L. rhamnosus GG persisted in biopsies taken from the colonic mucosa for up to 21 days at 7 × 104 CFU/biopsy sample after consumption ceased. Concluded from these studies, fecal cell counts are not a true reflection of the number of viable cells in the GIT of humans and should be accompanied with intestinal biopsies at sites of colonization.

Competitive exclusion of enteric pathogens

The term competitive exclusion was first used by Greenberg (1969) to describe the exclusion of S. typhimurium from blowfly maggots. This anti-pathogenic mechanism describes the scenario in which one bacterial species rigorously competes for adhesion to receptors in the GIT. The mechanisms of action used by one bacterial species to exclude another from the GIT differ and may include microbe-microbe interactions mediated by binding to the host mucosal interface at specific attachment sites, the secretion of antimicrobial substances and competition for available nutrients.,,,

For enteropathogens to initiate infection, they have to cross the intestinal mucosal barrier before colonizing the GIT. Once pathogens have penetrated the mucus layer overlying the intestinal epithelium, they attach to binding sites on epithelial cells. Attachment is followed by intestinal colonization and infection. Probiotics with adhesion capabilities protect the gut against enteric infections by preventing the attachment of pathogens Figure 1. Results from in vitro studies using human or animal mucosal material have demonstrated the effect of probiotic LAB on the competitive exclusion of pathogens.,, Lactobacillus rhamnosus GG has excellent adhesion properties and prevented the internalization of enterohemorrhagic E. coli (EHEC) in human intestinal cell lines. Enteric pathogens, such as EHEC, use mannose-sensitive type 1 fimbriae to attach to oligosaccharide residues of glycoproteins or glycolipids on the surface of intestinal epithelial cells (IECs). Probiotic strains of lactobacilli and bifidobacteria attach to the same receptor sites and exclude pathogens from binding to the GIT., Some probiotic strains have specific adhesion proteins on their cell surface that bind to carbohydrate moieties in the mucous layer, such as the mannose-specific adherence mechanism of L. plantarum.,, In some cases, competitive exclusion may be as simple as steric hindrance. An overview of studies that analyzed the effect of probiotic LAB surface proteins on adhesion and competitive exclusion using mutant analysis is provided in Table 3. One example of a specific adhesion protein involved in competitive exclusion adhesion-receptor interactions in the GIT is the L. plantarum mannose-specific adhesion (Msa) protein. A spontaneously mutated strain of the probiotic L. plantarum 299 v, thought to be affected in the msa gene, was unable to inhibit the attachment of EHEC to HT-29 epithelial cells compared to the wild-type. This suggested that Msa-containing probiotic strains could effectively exclude several other, if not all, type 1 fimbriated enteropathogens. Recently, Van Zyl et al. demonstrated the involvement of the mucus-adhesion protein (mapA) of L. plantarum 423 in competitive exclusion of Listeria monocytogenes EGDe in vivo, using gene knockout analysis and BLI. The mapA negative mutant strain of L. plantarum 423 was unable to exclude L. monocytogenes EGDe.

Another example of a putative competitive exclusion factor is the collagen-binding protein of L. fermentum. Heinemann et al. characterized the collagen surface-binding protein of L. fermentum RC-14, which inhibited the adherence of E. faecalis 1131. Other studies have demonstrated the role of surface layer (S-layer) extracts in the prevention of pathogens from attaching to, and thus colonizing, IECs., Chen et al. showed that S-layer proteins anchored on the cell surface of Lactobacillus crispatus ZJ001 were responsible for competitive exclusion of S. typhimurium and EHEC. Similar results were recorded by Johnson-Henry et al. The authors showed that S-layer protein extracts from Lactobacillus helveticus R0052 inhibited the adhesion of E. coli O157:H7 to Caco-2 cells. S-layer proteins are highly hydrophobic and it was suggested that pathogen adherence inhibition was mediated by hydrophobic group interactions as opposed to adhesion-receptor interactions.

Previous studies suggested that sortase-dependent cell surface proteins (SDPs) play a crucial role in probiotic-host interactions, adherence and colonization. Several SDPs have been identified with a role in in vitro and in vivo adhesion to intestinal cells, including mucus-binding cell surface proteins Table 3. In Gram-positive bacteria, sortases decorate the cell surface with a diverse array of proteins by covalently joining them to the cell wall (Sortase A) or by polymerizing proteins to construct complex multi-subunit pilin structures (Sortase C) on the cell surface. Sortases are characterized as cysteine transpeptidases that join SDPs containing a specific cell wall sorting signal (CWSS) to an amino group located on the cell surface. Sortase A enzymes anchor proteins that contain a CWSS with a LPXTG (where X donates any amino acid) C-terminal motif to the cell surface. The LPXTG motif is recognized by the SrtA enzyme, which breaks the threonine and glycine peptide bond and then covalently links the threonine residue to the amino group of the pentaglycine bacterial cell wall cross bridge., Sortase C proteins catalyze a similar transpeptidation reaction, but recognize a QVPTGV sorting motif to construct pili that promote microbial adhesion. Using mutant analysis coupled with in vivo BLI, a recent study showed that E. mundtii ST4SA sortase mutants (srtA and srtC) had a reduced ability to exclude L. monocytogenes EGDe from the GIT of mice compared to the wild-type derivative.

Several strains of lactobacilli and bifidobacteria inhibit, displace, and adhere to the same enterocyte layer as, enteropathogenic Salmonella choleraesuis serovar Typhimurium. This indicates that the probiotic strains have the ability to effectively displace the pathogen after pathogenic colonization of the gut has occurred instead of being effective only when administered in a preventative manner. To gain a competitive advantage, the probiotics can thus modify the gut environment by producing inhibitory compounds, lowering pH levels and competing for nutrients. Lactobacillus species such as L. acidophilus and L. plantarum have the ability to utilize complex carbohydrates such as fructans., Similarly, bifidobacteria are capable of metabolizing various plant dietary fibers using several depolymerizing enzymes. Utilizing carbohydrate sources other than those used by enteropathogenic bacteria enable probiotic bacteria to widen their areas of colonization in the GIT and inhibit pathogens.

Production of antimicrobial compounds

Antimicrobial compounds, produced by probiotic bacteria, can exert direct antimicrobial action toward competing enteropathogens that may lead to the prevention of pathogenic colonization of the GIT Figure 1b.

Bacteriocins

Bacteriocins are ribosomally produced antimicrobial peptides that differ in terms of their size (2–10 kDa) and mechanisms of action (for a review, see ref. 108). The production of bacteriocins by probiotic bacteria (usually LAB) is a key mechanism of action used to inhibit pathogens in the GIT. Bacteriocins usually only inhibit specific species, often those closely related to the producer., Some bacteriocins are reported to have a much broader spectrum of antimicrobial activity. Bacteriocins such as nisin, produced by Lc. lactis, plantaricin from L. plantarum and lacticin B from L. acidophilus are active against food-borne enteropathogens such as Listeria, Clostridium, Bacillus, methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci (VRE). Bacteriocins may have a bacteriostatic or direct bactericidal effect on pathogens, thus limiting the ability of the cells to colonize the gut. The associated antimicrobial activities of bacteriocins allow bacteriocin-producing probiotic strains to gain a competitive advantage within the complex GI environment.

Bacteriocins adhere to microbial cells and penetrate phospholipid membranes due to their small size and variations in hydrophobic and hydrophilic properties. The general mechanisms of bacteriocin-mediated pathogen killing include the induction of cytoplasmic membrane permeabilization of sensitive bacteria that leads to cell leakages, inhibition of DNA and RNA synthesis and/or cell wall protein-synthesis.,, For instance, nisin acts by forming a complex with the cell membrane lipid II precursor, followed by the aggregation and incorporation of peptides to form discrete pores in the bacterial cell membrane. A unique bacteriocin, bifidocin B, produced by Bifidobacterium bifidum NCFB, is active against several Gram-positive bacteria, including Listeria, Enterococcus, Bacillus and Lactobacillus, but shows no activity toward several other Gram-positive and Gram-negative bacteria. The difference in activity between strains is related to the ability of Gram-negative bacteria to resist adsorption of bifidocin B, due to their cell wall composition. However, several bacteriocins, such as mutacins (A-D), nisins (A and Z), lacticins (A164 and BH5), bacteriocins E 50–52 and OR7 are active against medically important Gram-negative organisms such as Campylobacter, Helicobacter, Haemophilus, Neisseria and Salmonella spp. In another study, a bacteriocin produced by Bacillus amyloliquefaciens RX7 showed broad-spectrum antibacterial, as well as antifungal, activity and inhibited the growth of Candida albicans, the causative agent of cutaneous candidiasis in humans. While the mode of action of bacteriocins against Gram-positive bacteria has been studied in depth, the direct mechanism of action of bacteriocins against Gram-negative bacteria is poorly understood., Tiwari et al. demonstrated the ability of bacteriocins enterocin E50-52, pediocin PA-1 and its hybrid peptides, EP and PE, to induce the efflux of intracellular ATP and to dissipate the cellular transmembrane potential of E. coli O157:H7 and S. enterica serovar Enteritidis 20E1090. Bacteriocins are mostly cationic peptides, and this characteristic enables electrostatic interactions with the negatively charged head groups of bacterial phospholipid. This is followed by insertion into the planar lipid bilayer or liposome membranes, leading to the formation of transient channels, leakage of cellular contents and subsequent cell death.

In addition to in vitro studies, several in vivo studies have demonstrated the inhibitory effect of purified bacteriocins and probiotic bacteriocin-producing strains in infectious animal models. Simonova et al. observed that feeding rabbits with bacteriocin-producing Enterococcus faecium CCM7420 and its partially purified bacteriocin significantly reduced Staphylococci spp. cell numbers in the cecum thus protecting the animals against infection. Other studies found that the E. faecium EK13, enterocin A producing strain reduced Salmonella cell numbers in gnotobiotic Japanese quails and reduced the colonization of pathogenic Staphylococcus in the digestive tract of rabbits., The capacity of human-isolated nisin- and pediocin-producing LAB to reduce the intestinal colonization of VRE in mice was demonstrated for the first time by Millette et al. Amyloliquecidin and penisin, produced by B. amyloliquefaciens and Paenibacillus sp. strain A3, respectively, significantly reduced methicillin resistant S. aureus (MRSA) infection levels in mice., Svetoch et al. reported a significant reduction of Salmonella enteritidis in broilers after oral administration of the E. faecium E 50–52 bacteriocin. Corr et al. demonstrated that feeding mice with the Lactobacillus salivarus UCC11 bacteriocin Abp118-producing strain reduced L. monocytogenes cell numbers in the liver and spleen. A similar reduction in cell numbers of the same pathogen in the GIT of mice was observed when the animals were pre-treated with probiotic strains L. plantarum 423 and E. mundtii ST4SA, producing bacteriocins plantaricin 423 and mundticin ST, respectively. Using gene knockout and reverse genetic analysis, the same authors confirmed bacteriocin production and adhesion proteins as mechanisms for the anti-listerial activity.

Several studies have demonstrated the topical application of bacteriocins to treat skin infections, mastitis and oral infections. Despite their powerful anti-infective therapeutic potential and a large selection of isolated and characterized bacteriocins, these peptides have not yet entered into clinical use. This is likely due to various production difficulties., However, progress in preclinical studies of several bacteriocins has proven promising. Several bacteriocins have been through different stages of preclinical development, targeting multi-drug resistant bacteria as well as cystic fibrosis. These include the bacteriocins, NVB302 and NVB333 (both produced by Actinoplanes liquriae NCIMB41362), mutacin 1140 (produced by Steptococcus mutans JH1000), NAI-107 (produced by Microbispora corallina) and Moli1901 (produced by Streptomyces cinnamoneum).

It is also important to consider that not all potential or developed probiotic strains that show in vitro antimicrobial activity against enteropathogens will be active in vivo. For example, despite the fact that a Lactobacillus sp. strain adhered to the jejunum and ileum of gnotobiotic pigs after oral administration and that the strain showed in vitro activity against enteropathogenic E. coli (EPEC), the strain failed to prevent EPEC colonization in the GIT of infected animals. Similar results were observed when L. casei subsp. casei failed to prevent the intestinal colonization of EPEC in the GIT of gnotobiotic or conventional piglets when the LAB strain was administered in a preventative setup. Nevertheless, most probiotics use their bacteriocins to effectively interact with enteropathogens through either bacteriostatic or bactericidal activities. In doing so, they prevent pathogenic colonization of the host GIT and subsequent occurrence of disease.

Bacteriocin-like inhibitory substances

Bacteriocin-like inhibitory substances (BLIS) have a broader spectrum of antimicrobial activity. Many of these compounds are not fully characterized or do not share characteristics typical of bacteriocins. The antimicrobial activities are not related to the production of lactic acid, other organic acids, or hydrogen peroxide., Lactobacillus rhamnosus GG secretes an antimicrobial substance with inhibitory activity against Clostridium spp., Staphylococcus spp., Enterobacteriaceae, Streptococcus spp., Bacteriodes spp., and Pseudomonas spp. This low molecular weight (LMW) substance is characterized as heat-stable, distinct from lactic and acetic acids, and closely resembles a microcin that is normally produced by Enterobacteriaeae spp. These characteristics suggest that it could be a BLIS. Similar substances with molecular weights and broad activity spectrums uncharacteristic of bacteriocins are produced by other lactobacilli, including strains of L. acidophilus and L. delbrueckii, their bactericidal affects are related to neither lactic acid nor hydrogen peroxide., Other studies have identified bacteriocin-like antimicrobial substances produced by several Bifidobacterium strains with broad spectrums of activity against both Gram-positive and Gram-negative pathogens such as L. monocytogenes, Salmonella spp. and E. coli spp.

Organic acids

An additional mechanism of pathogen displacement in the gut employed by probiotic bacteria is their ability to make the intestinal environment less suitable for pathogen growth. Probiotic LAB and commensal microbiota ferment carbohydrates in the GIT that lead to the production of metabolites such as acetic, formic, succinic and lactic acids, rendering the intestinal environment acidic and inhibiting the growth of bacterial pathogens. Organic acids, in particular lactic and acetic acid, repress the growth of many pathogenic bacteria in the GIT.,, The undissociated form of lactic acid functions as a permeabilizer of the Gram-negative bacterial outer cell membrane, after which it dissociates inside the bacterial cytoplasm following entry. The bacterial killing activity is exerted by lowering the intracellular pH level, through the accumulation of ionized forms of the organic acid and other antimicrobial compounds inside the cytoplasm.

De Keersmaecker et al. demonstrated that the strong inhibitory effects of L. rhamnosus GG against S. typhimurium was due to lactic acid production. Lehto and Salminen demonstrated the potential role of lactic acid in the ability of Lactobacillus strain GG to prevent the invasion of Caco-2 cells by S. enterica serovar Typhimurium. The authors suggested a pH-dependent mechanism after they observed that inhibition of the pathogen was eliminated when the LAB culture was set to pH 7. In another study, the growth and expression of the HilA and InvF virulence factors by Salmonella were affected by lactic acid.

The inhibition of E. coli O157:H7 by different Lactococcus and Lactobacillus strains was attributed to the production of lactic acid and low pH., The growth of Helicobacter pylori was inhibited by different Lactobacillus and Bifidobacterium strains including L. acidophilus, L. bulgaricus and Bifidobacterium bifidus., These effects were linked to the production of lactic, acetic and hydrochloric acid. In another study, the growth of four species of known enteropathogens, H. pylori, Campylobacter jejuni, Campylobacter coli and C. difficile was inhibited by Lactobacillus strains isolated from the human GIT, probably due to the production of organic acids. Based on these studies, it is reasonable to suggest that the production of organic acids by probiotics in the GIT makes the intestinal environment less favorable for their competitors and decreases the risk of enteric infections by pathogens.

Hydrogen peroxide

In addition to lactic acid and bacteriocin production, hydrogen peroxide (H2O2) production by commensal or probiotic LAB may be an important antimicrobial mechanism against pathogens. Hydrogen peroxide may cause reduced pathogen virulence, reduced pathogen invasion of epithelial cells or death of intestinal pathogens after epithelial intracellular diffusion which alters gene transcription and signal transduction., Several H2O2-producing bacterial species with probiotic properties have been isolated, such as B. bifidum, the Lactobacillus johnsonii NCC 533 gut isolate, a L. delbrueckii subsp. bulgaricus yogurt isolate and normal microflora vaginal isolates such as L. crispatus and L. gasseri.

The ability of L. johnsonii NCC533 to generate up to millimolar quantities of H2O2 under aerobic conditions has been demonstrated. The authors demonstrated the antimicrobial role of L. johnsonii NCC533 produced H2O2 against S. enterica serovar Typhimurium in vitro, and proposed that L. johnsonii NCC533 H2O2-production could contribute to protection against the pathogen in vivo. Other studies have shown that H2O2-producing L. crispatus F117 and Lactobacillus paracasei strains (F2 and F28) inhibited the growth of S. aureus in vitro., The beneficial role of H2O2-producing probiotic LAB that form part of the vaginal microflora of healthy women has been studied extensively. Previous studies have reported that women carrying H2O2-producing lactobacilli are less likely to develop bacterial vaginosis.,

Siderophores

Iron is an essential micronutrient that plays a central role in the metabolism and proliferation of most gut microbes, including commensal bacteria and gut pathogens. Siderophores are LMW, organic, high-affinity iron-chelating compounds produced by microorganisms such as bacteria and fungi. These compounds inhibit the growth, proliferation and persistence of competing microbes by depriving them of iron. In doing so, siderophore-producing bacteria sequester free iron available in their environment that is essential to other microorganisms. For example, the growth of Lc. lactis, C. difficile and Clostridium perfringens was inhibited in the GIT by iron-binding Bifidobacterium strains that produce siderophores. Growth and adhesion of enteropathogenic S. typhimurium N15 and EHEC to IECs were inhibited by B. pseudolongum PV8-2 and Bifidobacterium kashiwanohense PV20-2 with high iron sequestration properties.

Biosurfactants

The production of biosurfactants by some LAB is another mechanism that can interfere with pathogen growth in the GIT. Biosurfactants are a group of compounds with surface and emulsifying activities used in many different biomedical applications., Several LAB strains have been isolated that produce either cell-bound or secreted biosurfactants with antibacterial, antiviral and antifungal properties. Biosurfactants cause permeabilization of cells by effecting changes that disrupt or lyse the physical cell membrane structure. The use of biosurfactant-producing lactobacilli in the prevention of urogenital tract infections is of considerable interest. These organisms are believed to compete with urogenital bacterial pathogens and yeast for adhesion sites on epithelial cells and control their growth by the production of biosurfactants. In another study, L. casei MRTL3 that produces a bacteriocin and a biosurfactant, inhibited a broad range of pathogens, including L. monocytogenes, S. aureus, Shigella flexneri and Pseudomonas aeruginosa.

Compounds inhibiting pathogen adhesion to intestinal cells

Adhesion to intestinal cells and subsequent colonization by enteropathogens is regarded a prerequisite for virulence. Probiotic bacteria produce compounds that do not have a direct bactericidal effect, but contribute to the normal anti-infectious activities of the GIT by inhibiting the binding of pathogenic bacteria to the mucosal surface. Fujiwara et al. purified and characterized a novel proteinaceous compound in culture supernatants of B. longum SBT2928, termed BIF, that inhibits the adhesion of enterotoxigenic E. coli Pb176 (ETEC) to human HCT-8 IECs. The authors demonstrated that BIF blocks the binding of the ETEC Pb176 colonization factor antigen (CFA) II adhesive factor to gangliotetraosylceramide (bacterial binding structure) receptors on the intestinal cell surface, thereby preventing ETEC Pb176 colonization. Two Bifidobacterium strains, CA1 and F9, isolated from the GIT of infants produce a LMW, lipophilic, antibacterial compound that inhibits the adhesion of several pathogenic bacteria, including S. typhimurium SL1344 and E. coli C1845.

Stabilization of intestinal epithelial barrier

The GI epithelium consists of a uni-layer of cells covered by a mucus layer that is constantly exposed to the luminal contents and various enteric bacteria., The intestinal epithelial barrier consists of the mucus layer, the intestinal cells and the gut innate immune system. This GI barrier functions as a key defense mechanism required to maintain epithelial integrity and to prevent infection by pathogens and excessive inflammation. Stabilization and maintenance of this barrier is thus of utmost importance to the host. Important defense mechanisms of the intestinal barrier against unwelcome intrusion of harmful antigens include the mucosal layer (mucin production), intercellular junctional complexes (tight and adherence junctions) and the secretion of antimicrobial peptides (such as defensins) and immunoglobulin A (IgA). Disruption of this barrier function can lead to inappropriate inflammatory responses due to invasion of the submucosa by bacteria or food antigens, which may result in intestinal disorders such as inflammatory bowel disease (IBD) and ulcerative colitis.,, Consumption of colonizing or non-colonizing probiotics can enhance barrier integrity which helps to protect the intestinal epithelium against enteric pathogens and chronic inflammation by direct effects on the epithelium (e.g. increasing mucin expression by goblet cells), modulation of the immune system and by direct effects on commensal and pathogenic bacteria (e.g. antimicrobial peptides and competition for adherence) Figures 1 and 2.

Intestinal epithelium cells are overlaid with a protective inner and outer mucus layer that limits bacterial movement and acts as a dynamic defense barrier against enteropathogens and other potentially harmful antigens. For enteropathogens to colonize the intestine, they have to penetrate the mucus layer before they reach the intestinal epithelium. Mucins are the major macromolecular constituents of the epithelial mucus layer and are produced by specialized goblet cells in the intestinal tract. Probiotics are able to inhibit pathogen adherence to IECs by promoting the secretion of intestinal mucins and defensins Figure 1a. Several Lactobacillus species have been shown to increase the expression of specific mucin genes in human intestinal Caco-2 and HT29 cells, thus preventing the adherence and internalization of pathogenic E. coli.,, The adherence of EPEC was inhibited by L. plantarum 299 v-mediated increase in expression of the MUC2 and MUC3 mucins., Rats administered with VSL3 (pre- and probiotic mixture) for 7 consecutive days showed a 60-fold increase in MUC2 expression and an associated increase in mucin production. Therefore, increased mucus production mediated by probiotic bacteria in vivo may be a key mechanism in their interactions with enteropathogens to prevent infections and to improve intestinal barrier function.

Co-aggregation

Probiotic bacteria can prevent enteropathogenic adherence and intestinal colonization by co-aggregating with pathogens. In this process, probiotic bacteria interact closely with pathogens, allowing them the opportunity to release their anti-pathogenic substances in proximity to the pathogens. Probiotic LAB can form multi-cellular aggregates that are crucial for colonization of the oral cavity, the urogenital tract and the GIT.,, The ability of probiotic cells to co-aggregate is characterized by the clumping of cells that are genetically distinct, whereas auto-aggregation involves cells of the same strain., Auto- and co-aggregation have been reported for various Lactobacillus species, including L. plantarum, L. reuteri, L. gasseri, L. crispatus and L. coryniformis., Several studies have shown that the auto- and co-aggregation abilities of probiotic cells enhances their colonization and may enable the formation of a barrier to prevent colonization by pathogens., Lactobacillus plantarum strains (S1, A and B) co-aggregate with selected food-borne pathogens including S. typhimurium and L. monocytogenes. Lactobacillus plantarum S1 co-aggregated best with EHEC at 41.5%, L. plantarum A co-aggregated with S. Typhimurium at 40.5% and L. plantarum B co-aggregated with L. monocytogenes at 37.4%. This is a clear indication that the ability of LAB strains to bind to the food-borne pathogens is not restricted to one species or a single strain. In another study, the adherence of ETEC to porcine enterocytes was affected by co-aggregation of the pathogen with selected Lactobacillus spp., including L. fermentum, L. salivarius and L. delbrueckii.

The co-aggregation ability of probiotic LAB is generally related to a great diversity of properties among cell surface adherence proteins., Kos et al. demonstrated that differences in the hydrophobicity and hydrophilicity of the structural cell surface of L. acidophilus M9, L. plantarum L4 and E. faecium L3 may be responsible for the abilities of the strain to co-aggregate. In other examples, proteins involved in the maintenance of cell shape including the S-layer protein CbsA of L. crispatus JCM 5810, the DEAD box helicase AggH of L. reuteri 1063 and Apf of L. gasseri 4B2 were all responsible for the mediation of auto-aggregation. This suggests that the co-aggregation phenomenon of probiotic LAB may be a secondary activity of cell surface components involving random interactions with other surface components. Schachtsiek et al. described the role of a Lactobacillus coryniformis DSM 20001 surface protein encoded by a cpf gene (co/aggregation-promoting factor) in the ability of the LAB strain to co-aggregate with E. coli K-88, C. coli and C. jejuni. The auto- and co-aggregation ability of L. acidophilus M92 was shown to be mediated by proteinaceous surface layer (S-layer) components, approximated at 45 kDA in size.

Co-aggregation of probiotic and pathogenic bacteria is also mediated via the attachment of probiotic cells to fimbriae expressed on the cell surface of pathogens. This makes sense, as several studies have shown that probiotic LAB can prevent enteropathogenic binding to intestinal epithelial cells by attaching to the same carbohydrate receptor sites as the pathogens.,,, The attachment of probiotic cells to the surface of pathogenic cells is dependent on the specific type of fimbriae expressed by the pathogen. The expression of fimbriae by pathogens is important in colonization of the GIT, the vagina and perineum.,,, For example, E. coli that express type I fimbriae are most commonly associated with urinary tract infections. Mizuno et al. presented E.coli fimbriae and lipopolysaccharide (LPS) as the essential mediators of the co-aggregation of L. casei NBRC 3831 with E. coli K-12. Spencer and Chesson showed that selected strains of lactobacilli co-aggregate with enterotoxigenic E. coli expressing K88 fimbriae, but not with a K88-negative knockout mutant strain.

Inhibition of flagella motility

Flagella are known to play an important role as a virulence factor in many bacterial pathogens. Flagella allow pathogenic bacteria to respond to attractant and repellent gradients and are crucial for attachment to, and invasion of, eukaryotic cells. Foodborne pathogens such as S. enterica serovar Typhimurium require actively rotating flagella to rapidly contact and to efficiently penetrate GI epithelial cells. Salmonella Typhimurium remained noninvasive in infected mice when treated with a potent antibody that inhibits flagellum-based motility. Probiotic bacteria can impair the flagella motility of enteropathogens, thus preventing pathogenic colonization of the gut.

Líeven-Le Moal et al. demonstrated that antidiarrhoeic L. acidophilus LB and its secreted products inhibited the entry of S. enterica serovar Typhimurium into human intestinal Caco-2 cells by disrupting the swimming motility of the diarrhea-associated enteropathogen. The authors showed that L. acidophilus LB secretes a heat stable LMW product that causes rapid depolarization of the S. Typhimurium SL1344 cytoplasmic membrane. The inhibitory activity did not affect bacterial viability or flagellum expression. The transient impairment of the swimming motility of S. Typhimurium SL1344 leads to a delay in the pathogen’s capacity to induce F-actin membrane remodeling and thus entry into intestinal Caco-2 cells. In another study, levels of translocated Salmonella were dramatically lower in mice orally infected with S. Typhimurium when treated with the cell free supernatant of live probiotic lactobacilli, compared to that of untreated mice. It is possible that the difference between cell numbers of treated and untreated groups is due to a delay in pathogen translocation across the intestinal epithelial barrier caused by the inhibition of Salmonella swimming motility. This in turn, exposed the pathogenic cells for extended periods to host defenses in the intestinal lumen that includes antimicrobial products from both the host cells and the microbiota.

Immune system modulation

It is well known that probiotic bacteria can exert regulatory effects on host innate and adaptive immune responses. These bacteria have the ability to modulate the functions of dendritic cells (DCs), monocytes/macrophages, and T and B lymphocytes, which enhances phagocytosis of invading gut pathogens., By stimulation of the host immune responses (specific and nonspecific), probiotic bacteria can displace pathogens in the GIT and prevent intestinal diseases.

Probiotic bacteria can interact with pathogens in the gut by antagonizing inflammatory responses induced by the gut pathogens. Inflammation allows pathogens to flourish at the expense of the natural microbiota and host intestinal health. Probiotic bacteria are able to trigger an anti-inflammatory response from the innate immune system by signaling DCs to secrete anti-inflammatory cytokines such as interleukin 10 (IL-10) Figure 2c., They can also elicit a decrease in pro-inflammatory cytokines during inflammation. Down-regulation of pro-inflammatory cytokine secretion from immune cells occurs as a result of probiotic bacterial interference with inflammatory signaling pathways such as nuclear factor-kappa B (NF-ƘB) and mitogen-activated protein kinases (MAPK) Figure 2a., The activation of these signaling pathways leads to the secretion of pro-inflammatory cytokines that can severely damage the intestinal epithelial barrier. NF-ƘB and MAPK signaling pathways are activated by enteric pathogens to stimulate the secretion of pro-inflammatory cytokines (e.g. IL-8), that lead to the recruitment of inflammatory immune cells (e.g. neutrophils) to the infected area resulting in severe inflammation, tissue damage and disease Figure 2b., Several studies have identified probiotic strains with the ability to suppress pro-inflammatory cytokine production to avoid pathogen-induced inflammation at infection sites., A study by Finamore et al. reported that Lactobacillus amylovorus DSM 16698 protected IECs against the pro-inflammatory response induced by ETEC K88 through the suppression of pro-inflammatory cytokines IL-8 and IL-1ß. Another study demonstrated the ability of L. casei OLL2768 to suppress the ETEC-induced pro-inflammatory response by inhibition of NF-ƘB and MAPK pathways that reduced pro-inflammatory cytokine levels.

Probiotics also play a role in the stimulation and production of antibodies in the gut, particularly immunoglobulin A (IgA) Figure 2d., Antibodies released in the intestinal lumen can inhibit pathogen adherence to IECs by interfering with adhesive cell receptors on the pathogen’s cell membrane. Previous studies have indicated that Saccharomyces boulardii and L. rhamnosus GG increased secretory IgA levels or immunoglobulin-secreting cell levels in the GIT., Other studies have reported that oral administration of probiotic lactobacilli increased IgA levels in children suffering from diarrhea, thereby shortening the duration of symptoms., Several probiotic strains can also modulate the host immune mechanisms by influencing phagocytosis of enteric pathogens by host immune phagocytic cells such as macrophages.,,,,,, The inhibition of enteropathogenic P. aeruginosa and L. monocytogenes in mice by a strain of L. casei correlates to an increase in abundance of macrophages. Furthermore, probiotic bacteria can affect phagocytotic cell activities not only in clinical situations but also in healthy subjects.

Conclusion

Elucidating the mechanisms of action of probiotic microorganisms is a difficult task given the complex nature of the human GI ecosystem. Probiotic mechanisms of action employed against enteric pathogens are diverse, heterogeneous and may be strain specific. This suggests that the mechanism(s) of action of one specific probiotic strain against a particular disease or pathogen cannot be generalized since different strains evoke different responses in the host. Thus, the health benefits conferred by one strain are not applicable to another strain, even within the same species. Understanding the full potential of probiotics for therapeutic or prophylactic applications against GI diseases requires thorough investigations of probiotic-host and probiotic-pathogen interactions. Enhanced understanding of these interactions will enable the identification of true probiotics to target specific enteric diseases. While a number of recent in vivo studies have demonstrated the mechanistic basis behind observed probiotic effects at the molecular level, greater emphasis is warranted in this area of probiotic research. Unraveling the intricacies of probiotic-host and probiotic-pathogen interactions will improve the in vitro selection of the best probiotics based on key properties such as bacteriocin production and adhesion genes. Moreover, an efficient probiotic should exhibit stimulation of the hosts’ immune system and ultimately, must have demonstrable beneficial health effects on the host. It is clear that the demonstration of key antimicrobial and protective probiotic mechanisms in vivo will allow for industry and consumers to choose scientifically validated probiotics for the prevention or treatment of various health problems.

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    Brigidi P, Swennen E, Vitali B, Rossi M, Matteuzzi D. PCR detection of Bifidobacterium strains and Streptococcus thermophilus in faeces of human subjects after oral bacteriotherapy and yogurt consumption. Int J Food Microbiol. 2003;81(3):203–209. doi:.

    Not in our library10.1016/s0168-1605(02)00245-3

  63. 63.

    Klijn N, Weerkamp AH, de Vos WM. Genetic marking of Lactococcus lactis shows its survival in the human gastrointestinal tract.. Appl Environ Microbiol. 1995;61(7):2771–2774. doi:.

    Not in our library10.1128/aem.61.7.2771-2774.1995

  64. 64.

    Dicks LMT, Botes M. Probiotic lactic acid bacteria in the gastrointestinal tract: health benefits, safety and mode of action. Benef Microbes. 2010;1:11–29.

    Not in our library10.3920/bm2009.0012

  65. 65.
    Noninvasive biophotonic imaging for studies of infectious disease · 2011
    No notice
  66. 66.

    Van Zyl WF, Deane SM, Dicks LMT. Reporter systems for in vivo tracking of lactic acid bacteria in animal model studies. Gut Microbes. 2015;6(5):291–299. doi:.

    Not in our library10.1080/19490976.2015.1086058

  67. 67.

    Ouwehand AC, Salminen S. The health effects of cultured milk products with viable and non-viable bacteria. Int Dairy J. 1998;8(9):749–758. doi:.

    Not in our library10.1016/s0958-6946(98)00114-9

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    Xiao SD, Zhang DZ, Lu H, Jiang SH, Liu HY, Wang GS, Xu GM, Zhang ZB, Lin GJ, Wang GL. Multicenter, randomized, controlled trial of heat-killedLactobacillus acidophilus LB in patients with chronic diarrhea. Adv Ther. 2003;20(5):253–260. doi:.

    Not in our library10.1007/bf02849854

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    Roy D, Delcenserie V. The protective role of probiotics in disturbed enteric microbiota. In: Malago JJ, Koninkx JFJG, Marinsek-Logar R, editors. Probiotic bacteria and enteric infections. Dordrecht (Netherlands): Springer; 2011. p. 221–261.

    Not in our library

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    Kullen MJ, Amann MM, O’Shaughnessy W, O’Sullivan DJ, Busta FF, Brady U. Differentiation of ingested bifidobacteria by DNA fingerprinting demonstrates the survival of an unmodified strain in the gastrointestinal tract of humans. J Nutr. 1997;127(1):89–94. doi:.

    Not in our library10.1093/jn/127.1.89

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    Siitonen S, Vapautalo H, Salminen S, Gordin A, Saxelin M, Wikberg R, Kirkola AL. Effect of lactobacillus GG yoghurt in prevention of antibiotic associated diarrhoea. Ann Med. 1990;22(1):57–59. doi:.

    Not in our library10.3109/07853899009147243

  72. 72.

    Goldin BR, Gorbach SL, Saxelin M, Barakat S, Gualtieri L, Salminen S. Survival ofLactobacillus species (strain GG) in human gastrointestinal tract. Dig Dis Sci. 1992;37(1):121–128. doi:.

    Not in our library10.1007/bf01308354

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    Mättö J, Fondèn R, Tolvanen T, von Wright A, Vilpponen-Salmela T, Satokari R, Saarela M. Intestinal survival and persistence of probiotic Lactobacillus and Bifidobacterium strains administered in triple-strain yoghurt. Int Dairy J. 2006;16(10):1174–1180. doi:.

    Not in our library10.1016/j.idairyj.2005.10.007

  74. 74.

    Alander M, Korpela R, Saxelin M, Vilpponen-Salmela T, Mattila-Sandholm T, von Wright A. Recovery of Lactobacillus rhamnosus GG from human colonic biopsies. Lett Appl Microbiol. 1997;24(5):361–364. doi:.

    Not in our library10.1046/j.1472-765x.1997.00140.x

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    Guarino A, Berni Canani R, Immacacolata Spagnuolo M, Albano F, Di Benedetto L. Oral bacterial therapy reduces the duration of symptoms and of viral excretion in children with mild diarrhoea. J Paed Gastro. 1998;25:516–519.

    Not in our library10.1097/00005176-199711000-00005

  76. 76.

    Millar MR, Bacon C, Smith SL, Walke V, Hall MA. Enteral feeding of premature infants with Lactobacillus GG.. Arch Dis Child. 1993;69(5 Spec No):483–487. doi:.

    Not in our library10.1136/adc.69.5_spec_no.483

  77. 77.

    Greenberg B. Salmonella suppression by known populations of bacteria in flies. J Bacteriol. 1969;99(3):629–635. doi:.

    Not in our library10.1128/jb.99.3.629-635.1969

  78. 78.

    Lièven-Le Moal V, Servin AL. The front line of enteric host defence against unwelcome intrusion of harmful microorganisms: mucins, antimicrobial peptides, and microbiota. Clin Microbiol Revs. 2006;19:315–337.

    Not in our library10.1128/cmr.19.2.315-337.2006

  79. 79.

    Cossart P. Bacterial invasion: the paradigms of enteroinvasive pathogens. Sci. 2004;304(5668):242–248. doi:.

    Not in our library10.1126/science.1090124

  80. 80.

    Bibiloni R, Pérez PF, de Antoni GL. Will a high adhering capacity in a probiotic strain guarantee exclusion of pathogens from intestinal epithelia? Anaerobe. 1999;5(5):519–524. doi:.

    Not in our library10.1006/anae.1999.0198

  81. 81.

    Hirano J, Yoshida T, Sugiyama T, Koide N, Mori I, Yokochi T. The effect of lactobacillus rhamnosus on enterohemorrhagic escherichia coli infection of human intestinal cells in vitro. Microbiol Immunol. 2003;47(6):405–409. doi:.

    Not in our library10.1111/j.1348-0421.2003.tb03377.x

  82. 82.

    Tuomola EM, Ouwehand AC, Salminen S. The effect of probiotic bacteria on the adhesion of pathogens to human intestinal mucus. FEMS Immunol Med Microbiol. 1999;26(2):137–142. doi:.

    Not in our library10.1111/j.1574-695x.1999.tb01381.x

  83. 83.

    Hirn J, Nurmi E, Johansson T, Nuotio L. Long-term experience with competitive exclusion and salmonellas in Finland. Int J Food Microbiol. 1992;15(3–4):281–285. doi:.

    Not in our library10.1016/0168-1605(92)90059-c

  84. 84.

    Le Bouguenec C. Adhesins and invasins of pathogenic Escherichia coli. Int J Med Microbiol. 2005;295(6–7):471–478. doi:.

    Not in our library10.1016/j.ijmm.2005.07.001

  85. 85.

    Nesser JR, Granato D, Rouvet M, Servin A, Teneberg S, Karlsson KA. Lactobacillus johnsonii La1 shares carbohydrate-binding specificities with several enteropathogenic bacteria. Glycobiol. 2000;10(11):1193–1199. doi:.

    Not in our library10.1093/glycob/10.11.1193

  86. 86.

    Mukai T, Asasaka T, Sato E, Mori K, Matsumoto M, Ohori H. Inhibition of binding of Helicobacter pylori to the glycolipid receptors by probiotic Lactobacillus reuteri. FEMS Immunol Med Microbiol. 2002;32:105–110.

    Not in our library10.1111/j.1574-695x.2002.tb00541.x

  87. 87.

    Ofek I, Doyle RJ. Bacterial adhesion to cells and tissues. New York (USA): Chapman and Hall; 1994.

    Not in our library

  88. 88.

    Coconnier MH, Bernet MF, Chauviere G, Servin AL. Adhering heat-killed human Lactobacillus acidophilus strain LB inhibits the process of pathogenicity of diarrhoeagenic bacteria in cultured human intestinal cells. J Diarrhoeal Dis Res. 1993;11:235–242.

    Not in our library

  89. 89.

    Pretzer G, Snel J, Molenaar D, Wiersma A, Bron PA, Lambert J, de Vos WM, van der Meer R, Smits MA, Kleerebezem M. Biodiversity-based identification and functional characterization of the mannose-specific adhesin of lactobacillus plantarum. J Bacteriol. 2005;187(17):6128–6136. doi:.

    Not in our library10.1128/jb.187.17.6128-6136.2005

  90. 90.

    Bron PA, Meijer M, Bongers RS, de Vos WM, Kleerebezem M. Dynamics of competitive population abundance of Lactobacillus plantarum ivi gene mutants in faecal samples after passage through the gastrointestinal tract of mice. J Appl Microbiol. 2007;103:1424–1434.

    Not in our library10.1111/j.1365-2672.2007.03376.x

  91. 91.

    Mack DR, Ahrne S, Hyde L, Wei S, Hollingsworth MA. Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro. Gut. 2003;52(6):827–833. doi:.

    Not in our library10.1136/gut.52.6.827

  92. 92.

    Buck BL, Altermann E, Svingerud T, Klaenhammer TR. Functional analysis of putative adhesion factors in Lactobacillus acidophilus NCFM. Appl Environ Microbiol. 2005;71(12):8344–8351. doi:.

    Not in our library10.1128/aem.71.12.8344-8351.2005

  93. 93.

    van Pijkeren JP, Canchaya C, Ryan KA, Li Y, Claesson MJ, Sheil B, Steidler L, O’Mahony L, Fitzgerald GF, van Sinderen D, et al. Comparative and functional analysis of sortase-dependent proteins in the predicted secretome of Lactobacillus salivarius UCC118. Appl Environ Microbiol. 2006;72(6):4143–4153. doi:.

    Not in our library10.1128/aem.03023-05

  94. 94.

    Walter J, Chagnaud P, Tannock GW, Loach DM, Dal Bello F, Jenkinson HF, Hammes WP, Hertel C. A high-molecular-mass surface protein (Lsp) and methionine sulfoxide reductase B (MsrB) contribute to the ecological performance of Lactobacillus reuteri in the murine gut. Appl Environ Microbiol. 2005;71(2):979–986. doi:.

    Not in our library10.1128/aem.71.2.979-986.2005

  95. 95.

    Heinemann C, Vlieg JETV, Janssen DB, Busscher HJ, van der Mei HC, Reid G. Purification and characterization of a surface-binding protein from Lactobacillus fermentum RC-14 that inhibits adhesion of Enterococcus faecalis 1131. FEMS Microbiol Lett. 2000;190(1):177–180. doi:.

    Not in our library10.1111/j.1574-6968.2000.tb09282.x

  96. 96.

    Chen XY, Xu JJ, Shuai JB, Chen JS, Zhang ZF, Fang WH. The S-layer proteins of Lactobacillus crispatus strain ZJ001 is responsible for competitive exclusion against Escherichia coli O157: H7 and Salmonella typhimurium. Int J Food Microbiol. 2007;115(3):307–312. doi:.

    Not in our library10.1016/j.ijfoodmicro.2006.11.007

  97. 97.

    Johnson-Henry KC, Hagen KE, Gordonpour M, Tompkins TA, Sherman PM. Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157: h7adhesion to epithelial cells. Cell Microbiol. 2007;9(2):356–367. doi:.

    Not in our library10.1111/j.1462-5822.2006.00791.x

  98. 98.

    Boekhorst J, De Been MWHJ, Kleerebezem M, Siezen RJ. Genome-wide detection and analysis of cell wall-bound proteins with LPxTG-like sorting motifs. J Bacteriol. 2005;187(14):4928–4934. doi:.

    Not in our library10.1128/jb.187.14.4928-4934.2005

  99. 99.

    Spirig T, Weine EM, Clubb RT. Sortase enzymes in Gram-positive bacteria. Mol Microbiol. 2011;82(5):1044–1059. doi:.

    Not in our library10.1111/j.1365-2958.2011.07887.x

  100. 100.

    Clancy KW, Melvin JA, McCafferty DG. Sortase transpeptidases: insights into mechanism, substrate specificity, and inhibition. Biopolymers. 2010;94(4):385–396. doi:.

    Not in our library10.1002/bip.21472

  101. 101.

    Navarre WW, Schneewind O. Surface proteins of Gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev. 1999;63:174–229.

    Not in our library10.1128/mmbr.63.1.174-229.1999

  102. 102.

    Barnett TC, Patel AR, Scott JR. A novel sortase, SrtC2, from Streptococcus pyogenes anchors a surface protein containing a QVPTGV motif to the cell wall. J Bacteriol. 2004;186(17):5865–5875. doi:.

    Not in our library10.1128/jb.186.17.5865-5875.2004

  103. 103.

    Candela M, Perna F, Carnevali P, Vitali B, Ciati R, Gionchetti P, Rizzello F, Campieri M, Brigidi P. Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 productions. Int J Food Microbiol. 2008;125(3):286–292. doi:.

    Not in our library10.1016/j.ijfoodmicro.2008.04.012

  104. 104.

    Walter J. Ecological role of lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Appl Environ Microbiol. 2008;74(16):4985–4996. doi:.

    Not in our library10.1128/aem.00753-08

  105. 105.

    Rossi M, Corradini C, Amaretti A, Nicolini M, Pompei A, Zanoni S, Matteuzi D. Fermentation of fructooligosaccharides and inulin by bifidobacteria: a comparative study in pure and faecal cultures. Appl Environ Microbiol. 2005;71(10):6150–6158. doi:.

    Not in our library10.1128/aem.71.10.6150-6158.2005

  106. 106.
    Biomanufacturing process for the production of bacteriocins from Bacillaceae family · 2020
    Not checked
  107. 107.

    van der Donk WA, Nair SK. Structure and mechanism of lanthipeptide biosynthetic enzymes. Curr Opin Struct Biol. 2014;29:58–66. doi:.

    Not in our library10.1016/j.sbi.2014.09.006

  108. 108.
    A Review: The Fate of Bacteriocins in the Human Gastro-Intestinal Tract: Do They Cross the Gut–Blood Barrier? · 2018
    Corrected
  109. 109.

    Smaoui S, Elleuch L, Bejar W, Karray-Rebai I, Ayadi I, Jaouadi B, Mathieu F, Chouayekh H, Bejar S, Mellouli L. Inhibition of fungi and Gram-negative bacteria by bacteriocin BacTN635 produced by Lactobacillus plantarum sp. TN635. Reproduction. 2009;128:117–126.

    Not in our library10.1007/s12010-009-8821-7

  110. 110.

    Drider D, Bendali F, Naghmouchi K, Chikindas M. Bacteriocins: not only antimicrobial agents. Probiot Antimicrob Prot. 2016;8(4):177–182. doi:.

    Not in our library10.1007/s12602-016-9223-0

  111. 111.

    Chikindas M, Weeks R, Drider D, Chistyakov V, Dicks LMT. Functions and emerging applications of bacteriocins. Curr Opin Biotechnol. 2017;49:23–28. doi:.

    Not in our library10.1016/j.copbio.2017.07.011

  112. 112.

    Fujiwara S, Hashiba H, Hirota T, Forstner JF. Proteinaceous factor(s) in culture supernatant fluids of bifidobacteria which prevents the binding of enterotoxigenic Escherichia coli to gangliotetraosylceramide.. Appl Environ Microbiol. 1997;63(2):506–512. doi:.

    Not in our library10.1128/aem.63.2.506-512.1997

  113. 113.

    Fujiwara S, Hashiba H, Hirota T, Forstner JF. Inhibition of the binding of enterotoxigenic Escherichia coli Pb176 to human intestinal epithelial cell line HCT-8 by an extracellular protein fraction containing BIF of Bifidobacterium longum SBT2928: suggestive evidence of blocking of the binding receptor gangliotetraosylceramide on the cell surface. Int J Food Microbiol. 2001;67:97–106.

    Not in our library10.1016/s0168-1605(01)00432-9

  114. 114.

    Singh VP. Recent approaches in food bio-preservation. Open Vet J. 2018;8(1):104–111. doi:.

    Not in our library10.4314/ovj.v8i1.16

  115. 115.

    De Kwaadsteniet M, Van Reenen C, Dicks LMT. Evaluation of nisin F in the treatment of subcutaneous skin infections, as monitored by using a bioluminescent strain of Staphylococcus aureus. Prob Antimicrob Prot. 2010;2(2):61–65. doi:.

    Not in our library10.1007/s12602-009-9017-8

  116. 116.

    Van Reenen C, Chikindas M, Van Zyl W, Dicks LMT. Characterization and heterologous expression of a class IIa bacteriocin, plantaricin 423 from Lactobacillus plantarum 423, in Saccharomyces cerevisiae. Int J Food Microbiol. 2003;81(1):29–40. doi:.

    Not in our library10.1016/s0168-1605(02)00164-2

  117. 117.

    Cotter PD, Ross RP, Hill C. Bacteriocins-a viable alternative to antibiotics? Nat Rev Microbiol. 2012;11(2):95–105. doi:.

    Not in our library10.1038/nrmicro2937

  118. 118.

    Ratchaneewan A, Pipatsatitpong D. Isolation and characterization of a bacteriocin with anti-MRSA activity from Bacillus sp. strain WASM9-25M. Thai J Pharmacol. 2014;36:19–28.

    Not in our library

  119. 119.

    Garg N, Oman TJ, Andrew Wang TS, De Gonzalo CV, Walker S, van der Donk WA. Mode of action and structure-activity relationship studies of geobacillin I. J Antibiot. 2014;67(1):133–136. doi:.

    Not in our library10.1038/ja.2013.112

  120. 120.

    O’Shea EF, Cotter PD, Stanton C, Ross RP, Hill C. Production of bioactive substances by intestinal bacteria as a basis for explaining probiotic mechanisms: bacteriocins and conjugated linoleic acid. Int J Food Microbiol. 2012;152(3):189–205. doi:.

    Not in our library10.1016/j.ijfoodmicro.2011.05.025

  121. 121.

    Izadpanah A, Gallo RL. Antimicrobial peptides. J Acad Dermatol. 2005;52(3):381–390. doi:.

    Not in our library10.1016/j.jaad.2004.08.026

  122. 122.

    Islam MR, Nagao JI, Zendo T, Sonomoto K. Antimicrobial mechanism of lantibiotics. Biochem Soc Trans. 2012;40(6):1528–1533. doi:.

    Not in our library10.1042/bst20120190

  123. 123.

    Nishie M, Nagao JI, Sonomoto K. Antibacterial peptides “bacteriocins”: an overview of their diverse characteristics and applications. Biocontrol Sci. 2012;17(1):1–16. doi:.

    Not in our library10.4265/bio.17.1

  124. 124.

    Bierbaum G, Sahl HG. Lantibiotics: mode of action, biosynthesis and bioengineering. Curr Pharm Biotechnol. 2009;10(1):2–18. doi:.

    Not in our library10.2174/138920109787048616

  125. 125.

    Yildirim Z, Johnson MG. Characterization and antimicrobial spectrum of bifidocin B, a bacteriocin produced by Bifidobacterium bifidum NCFB 1454. J Food Protect. 1998;61:47–51.

    Not in our library10.4315/0362-028x-61.1.47

  126. 126.

    Yildirim Z, Winters DK, Johnson MG. Purification, amino acid sequence and mode of action of bifidocin B produced by Bifidobacterium bifidum NCFB 1454. J Appl Microbiol. 1999;86(1):45–54. doi:.

    Not in our library10.1046/j.1365-2672.1999.00629.x

  127. 127.

    Kim TS, Hur JW, Yu MA, Cheigh CI, Kim KN, Hwang JK, Pyun YR. Antagonism of Helicobacter pylori by bacteriocins of lactic acid bacteria. J Food Protect. 2003;66(1):3–12. doi:.

    Not in our library10.4315/0362-028x-66.1.3

  128. 128.

    Stevens KA, Sheldon BW, Klapes NA, Klaenhammer TR. Nisin treatment for inactivation of Salmonella species and other gram-negative bacteria.. Appl Environ Microbiol. 1991;57(12):3613–3615. doi:.

    Not in our library10.1128/aem.57.12.3613-3615.1991

  129. 129.

    Svetoch EA, Levchuk VP, Pokhilenko VD, Eruslanov BV, Mitsevich EV, Mitsevich IP, Perelygin VV, Stephanshin YG, Stern NJ. Inactivating methicillin-resistant Staphylococcus aureus and other pathogens by use of bacteriocins OR-7 and E 50-52. J Clin Microbiol. 2008;46(11):3863–3865. doi:.

    Not in our library10.1128/jcm.01081-08

  130. 130.

    Morency H, Mota-Meira M, Lapointe G, Lacroix C, Lavoie MC. Comparison of the activity spectra against pathogens of bacterial strains producing a mutacin or a lantibiotic. Can J Microbiol. 2001;47(4):322–331. doi:.

    Not in our library10.1139/w01-013

  131. 131.

    Ghodbane H, Elaidi S, Sabatie J, Achour S, Regaya JI. Bacteriocins active against multi-resistant Gram-negative bacteria implicated in nosocomial infections. Infec Disorders-Drug Targets. 2015;15(1):2–12. doi:.

    Not in our library10.2174/1871526514666140522113337

  132. 132.

    Prudȇncio CV, Dos Santos MT, Vanetti MCD. Strategies for the use of bacteriocins in Gram-negative bacteria: relevance in food microbiology. J Food Sci Technol. 2015;52:5408–5417.

    Not in our library10.1007/s13197-014-1666-2

  133. 133.

    Lim KB, Balolong MP, Kim SH, Oh JK, Lee JY, Kang DK. Isolation and characterization of a broad spectrum bacteriocin from Bacillus amyloliquefaciens RX7. Biomed Res Int. 2016;2016:8521476.

    Not in our library10.1155/2016/8521476

  134. 134.

    Tiwari SK, Noll KS, Cavera VL, Chikindas ML, Macfarlane GT. Improved antimicrobial activities of synthetic-hybrid bacteriocins designed from enterocin E50-52 and pediocin PA-1. Appl Environ Microbiol. 2014;81(5):1661–1667. doi:.

    Not in our library10.1128/aem.03477-14

  135. 135.

    Duclohier H, Molle SG. Antimicrobial peptide magainin I from Xenopus skin forms anion-permeable channels in planar lipid bilayers. Biophys J. 1989;56(5):1017–1021. doi:.

    Not in our library10.1016/s0006-3495(89)82746-8

  136. 136.

    Kagan BL, Selsted ME, Ganz T, Lehrer RI. Antimicrobial defensin peptides form voltage-dependent ion-permeable channels in planar lipid bilayer membranes. Proc Natl Acad Sci USA. 1990;87(1):210–216. doi:.

    Not in our library10.1073/pnas.87.1.210

  137. 137.

    Simanova MP, Laukova A, Chrastinova L, Strompfova V, Faix S, Vasilkova Z, Ondruska L, Jurcik R, Rafay J. Enterococcus faecium CCM7420, bacteriocin PPB CCM7420 and their effect in the digestive tract of rabbits. Czech J Anim Sci. 2009;54(No. 8):376–386. doi:.

    Not in our library10.17221/1659-cjas

  138. 138.

    Laukova A, Guba P, Nemcova R, Vasilkova Z. Reduction of Salmonella in gnotobiotic Japanese quails caused by the enterocin A-producing EK13 strain of Enterococcus faecium. Vet Res Commun. 2003;27(4):275–280. doi:.

    Not in our library10.1023/a:1024027923824

  139. 139.

    Laukova A, Strompfova V, Skrikvanova V, Volek Z, Jindrichova E, Marounek M. Bacteriocin-producing strain of Enterococcus faecium EK13 with probiotic characteristics and its application in the digestive tract of rabbits. Biol Bratisl. 2006;61(6):779–782. doi:.

    Not in our library10.2478/s11756-006-0191-9

  140. 140.

    Van Staden AD, Heunis T, Smith C, Deane SM, Dicks LMT. Efficacy of lantibiotic treatment of staphylococcus aureus-induced skin infections, monitored by in vivo bioluminescent imaging. Antimicrob Agents Chemother. 2016;60(7):3948–3955. doi:.

    Not in our library10.1128/aac.02938-15

  141. 141.

    Baindara P, Chaudhry V, Mittal G, Liao LM, Matos CO, Franco OL, Patil PB, Korpole S. Characterization of the antimicrobial peptide penisin, a class Ia novel lantibiotic from Paenibacillus sp. strain A3. Antimicrob Agents Chemother. 2015;60(1):580–591. doi:.

    Not in our library10.1128/aac.01813-15

  142. 142.

    Svetoch AE, Eruslanov BV, Pereglygin VV, Mitsevich EV, Mitsevich IP, Borzenkov VN, Levchuk VP, Svetoch OE, Kovalev YN, Stephanshin YG, et al. Diverse antimicrobial killing by enterococcus faecium E 50-52 bacteriocin. J Agric Food Chem. 2008;6(6):1942–1948. doi:.

    Not in our library10.1021/jf073284g

  143. 143.

    Heunis TD, Smith C, Dicks LMT. Evaluation of a nisin-eluting nanofiber scaffold to treat staphylococcus aureus-induced skin infections in mice. Antimicrob Agents Chemother. 2013;57(8):3928–3935. doi:.

    Not in our library10.1128/aac.00622-13

  144. 144.

    Fernández L, Delgado S, Herrero H, Maldonado A, Rodrȋguez JM. The bacteriocin nisin, an effective agent for the treatment of staphylococcal mastitis during lactation. J Hum Lact. 2008;24(3):311–316. doi:.

    Not in our library10.1177/0890334408317435

  145. 145.

    Turner S, Loveand R, Lyons K. An in vitro investigation of the antibacterial effect of nisin in root canals and canal wall radicular dentine. Int Endod J. 2004;37(10):664–671. doi:.

    Not in our library10.1111/j.1365-2591.2004.00846.x

  146. 146.

    Hillman J, Mo J, McDonell E, Cvitkovitch D, Hillman C. Modification of an effector strain for replacement therapy of dental caries to enable clinical safety trials. J Appl Microbiol. 2007;102(5):1209–1219. doi:.

    Not in our library10.1111/j.1365-2672.2007.03316.x

  147. 147.

    Dobson A, O’Connor P, Cotter P, Ross R, Hill C. Impact of the broad-spectrum antimicrobial peptide, lacticin 3147, on Streptococcus mutans growing in a biofilm and in human saliva. J Appl Microbiol. 2011;111(6):515–1523. doi:.

    Not in our library10.1111/j.1365-2672.2011.05153.x

  148. 148.

    Legala OE, Yassi H, Pflugmacher S, Neubauer P. Pharmacological and pharmacokinetic properties of lanthipeptides undergoing clinical studies. Biotechnol Lett. 2017;39(4):473–482. doi:.

    Not in our library10.1007/s10529-016-2279-9

  149. 149.

    Legala OE, Neubauer P. Lanthipeptides: chemical synthesis versus in vivo biosynthesis as tools for pharmaceutical production. Microb Cell Fact. 2016;15(1):97. doi:.

    Not in our library10.1186/s12934-016-0502-y

  150. 150.

    Lopetuso LR, Giorgio ME, Saviano A, Scaldaferri F, Gasbarrini A, Cammarota G. Bacteriocins and bacteriophages: therapeutic weapons for gastrointestinal diseases? Int J Molec Sci. 2019;20(1):183. doi:.

    Not in our library10.3390/ijms20010183

  151. 151.

    Sandiford SK. Perspectives on lantibiotic discovery-Where have we failed and what improvements are required? Exp Opin Drug Disc. 2015;10(4):315–320. doi:.

    Not in our library10.1517/17460441.2015.1016496

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    Bomba A, Nemcova R, Kastel R, Herich R, Pataky J, Cizek M. Interactions of Lactobacillus spp. and enteropathogenic Escherichia coli under in vitro and in vivo conditions. Vet Med. 1996;41:155–158.

    Not in our library

  153. 153.

    Bomba A, Nemcova R, Gancarcikova S, Herich R, Kastel R. Potentiation of the effectiveness of Lactobacillus casei in the prevention of E. coli induced diarrhoea in conventional and gnotobiotic pigs. Adv Exp Med Biol. 1999;473:185–190.

    Not in our library10.1007/978-1-4615-4143-1_18

  154. 154.

    Malago JJ, Koninkx JFJG. Probiotic-pathogen interactions and enteric cytoprotection. In: Malago JJ, Koninkx JFJG, Marinsek-Logar R, editors. Probiotic bacteria and enteric infections. Dordrecht (Netherlands): Springer; 2011. p. 289–311.

    Not in our library

  155. 155.

    Silva M, Jacobus N, Deneke C, Gorbach SL. Antimicrobial substance from a human Lactobacillus strain.. Antimicrob Agents Chemother. 1987;31(8):1231–1233. doi:.

    Not in our library10.1128/aac.31.8.1231

  156. 156.

    Van De Guchte M, Ehrlich SD, Maguin E. Production of growth-inhibiting factors by Lactobacillus delbrueckii. J Appl Microbiol. 2001;91(1):147–153. doi:.

    Not in our library10.1046/j.1365-2672.2001.01369.x

  157. 157.

    Bernet-Camard MF, Lievin V, Brassart D, Neeser JR, Servin AL, Hudault S. The human Lactobacillus acidophilus strain LA1 secretes a nonbacteriocin antibacterial substance(s) active in vitro and in vivo.. Appl Environ Microbiol. 1997;63(7):2747–2753. doi:.

    Not in our library10.1128/aem.63.7.2747-2753.1997

  158. 158.

    O’Riordan K, Fitzferald GF. Evaluation of Bifidobacteria for the evaluation of antimicrobial compounds and assessment of performance in cottage cheese at refrigeration temperature. J Appl Microbiol. 1998;85(1):103–114. doi:.

    Not in our library10.1046/j.1365-2672.1998.00474.x

  159. 159.

    Bielecka M, Biedrycka E, Biedrycka E, Smoragiewicz W, Smieszek M. Interaction of Bifidobacterium and Salmonella during associated growth. Int J Food Microbiol. 1998;45(2):151–155. doi:.

    Not in our library10.1016/s0168-1605(98)00150-0

  160. 160.

    Lee YJ, Yu WK, Heo TR. Identification and screening for antimicrobial activity against clostridium difficile of bifidobacterium and lactobacillus species isolated from healthy infant faeces. Int J Antimicrob Agents. 2003;21(4):340–346. doi:.

    Not in our library10.1016/s0924-8579(02)00389-8

  161. 161.

    Van den Bergh PA. Lactic acid bacteria, their metabolic products and interference with microbial growth. FEMS Microbiol Rev. 1993;12(1–3):221–238. doi:.

    Not in our library10.1111/j.1574-6976.1993.tb00020.x

  162. 162.

    Alakomi HL, Skytta E, Saarela M, Mattila-Sandholm T, Latva-Kala K, Helander IM. Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. Appl Environ Microbiol. 2000;66(5):2001–2005. doi:.

    Not in our library10.1128/aem.66.5.2001-2005.2000

  163. 163.

    Russell JB, Diez-Gonzalez F. The effects of fermentation acids on bacterial growth. Adv Microb Physiol. 1998;39:205–234.

    Not in our library10.1016/s0065-2911(08)60017-x

  164. 164.

    De Keersmaecker SC, Verhoeven TL, Desair J, Marchal K, Vanderleyden J, Nagy I. Strong antimicrobial activity of Lactobacillus rhamnosus GG against Salmonella typhimurium is due to accumulation of lactic acid. FEMS Microbiol Lett. 2006;259(1):89–96. doi:.

    Not in our library10.1111/j.1574-6968.2006.00250.x

  165. 165.

    Lehto EM, Salminen SJ. Inhibition of Salmonella typhimurium adhesion to Caco-2 cell cultures by Lactobacillus strain GG spent culture supernate: only a pH effect? FEMS Immunol Med Microbiol. 1997;18(2):125–132. doi:.

    Not in our library10.1111/j.1574-695x.1997.tb01037.x

  166. 166.

    Durant JA, Corrier DE, Ricke SC. Short-chain volatile fatty acids modulate the expression of the hilA and invF genes of Salmonella typhimurium. J Food Prot. 2000;63(5):573–578. doi:.

    Not in our library10.4315/0362-028x-63.5.573

  167. 167.

    Brashears MM, Reilly SS, Gilliland SE. Antagonistic action of cells of Lactobacillus lactis toward Escherichia coli 0157: h7on refrigerated raw chicken meat. J Food Prot. 1998;61(2):166–170. doi:.

    Not in our library10.4315/0362-028x-61.2.166

  168. 168.

    Ogawa M, Shimizu K, Nomoto K, Tanaka R, Hamabata T, Yamasaki S, Takeda T, Takeda Y. Inhibition of in vitro growth of Shiga toxin-producing Escherichia coli O157: h7by probiotic Lactobacillus strains due to production of lactic acid. Int J Food Microbiol. 2001;68(1–2):135–140. doi:.

    Not in our library10.1016/s0168-1605(01)00465-2

  169. 169.

    Midolo PD, Lambert JR, Hull R, Luo F. In vitro inhibition of Helicobacter pylori NCTC 11637 by organic acids and lactic acid bacteria. J Appl Bacteriol. 1995;79(4):475–479. doi:.

    Not in our library10.1111/j.1365-2672.1995.tb03164.x

  170. 170.

    Bhatia SJ, Kochar N, Abraham P, Nair NG, Mehta AP. Lactobacillus acidophilus inhibits growth of Campylobacter pylori in vitro.. J Clin Microbiol. 1989;27(10):2328–2330. doi:.

    Not in our library10.1128/jcm.27.10.2328-2330.1989

  171. 171.

    Strus M, Pakosz K, Gosciniak H, Przondo-Mordarska A, Rozynek E, Pituch H, Meisel-Mikolajczyk F, Heczko PB. Antagonistic activity of Lactobacillus bacteria strains against anaerobic gastrointestinal tract pathogens (Helicobacter pylori, Campylobacter coli, Campylobacter jejuni, Clostridium difficile). Med Dosw Mikrobiol. 2001;53:133–142.

    Not in our library

  172. 172.

    Fayol-Messaoudi D, Berger CN, Coconnier-Polter MH, Lievin-Le Moal V, Servin AL. pH-, lactic acid-, and non-lactic acid-dependent activities of probiotic lactobacilli against Salmonella enterica serovar Typhimurium. Appl Environ Microbiol. 2005;71(10):6008–6013. doi:.

    Not in our library10.1128/aem.71.10.6008-6013.2005

  173. 173.

    Botteaux A, Hoste C, Dumont JE, Van Sande J, Allaoui A. Potential role of Noxes in the protection of mucosae: H2O2 as a bacterial repellent. Microbes Infect. 2009;11(5):537–544. doi:.

    Not in our library10.1016/j.micinf.2009.02.009

  174. 174.

    Knaus UG, Hertzberger R, Pircalabioru GG, Yousefi SPM, Dos Santos FB. Pathogen control at the intestinal mucosa - H2O2 to the rescue. Gut Microbes. 2017;8(1):67–74. doi:.

    Not in our library10.1080/19490976.2017.1279378

  175. 175.

    Alvarez LA, Kovacic L, Rodriguez J, Gosemann JH, Kubica M, Pircalabioru GG, Friedmacher F, Cean A, Ghişe A, Sărăndan MB, et al. NADPH oxidase-derived H2O2 subverts pathogen signalling by oxidative phosphotyrosine conversion to PB-DOPA. Proc Natl Acad Sci USA. 2016;113(37):10406–10411. doi:.

    Not in our library10.1073/pnas.1605443113

  176. 176.

    Pridmore RD, Pittet AC, Praplan F, Cavadini C. Hydrogen peroxide production by Lactobacillus johnsonii NCC 533 and its role in anti-Salmonella activity. FEMS Microbiol Lett. 2008;283(2):210–215. doi:.

    Not in our library10.1111/j.1574-6968.2008.01176.x

  177. 177.

    Kawasaki S, Satoh T, Todorok M, Niimura Y. b-type dihydroorotate dehydrogenase is purified as a H2O2-forming NADH oxidase from Bifidobacterium bifidum. Appl Environ Microbiol. 2009;75(3):629–636. doi:.

    Not in our library10.1128/aem.02111-08

  178. 178.

    Hertzberger R, Arents J, Dekker HL, Pridmore RD, Gysler C, Kleerebezem M, de Mattos MJT. H2O2 production in species of the Lactobacillus acidophilus group: a central role for a novel NADH-Dependent Flavin reductase. Appl Environ Microbiol. 2014;80:2229–2239.

    Not in our library10.1128/aem.04272-13

  179. 179.

    Marty-Teysset C, de la Torre F, Garel J. Increased production of hydrogen peroxide by Lactobacillus delbrueckii subsp. bulgaricus upon aeration: involvement of an NADH oxidase in oxidative stress. Appl Environ Microbiol. 2000;66(1):262–267. doi:.

    Not in our library10.1128/aem.66.1.262-267.2000

  180. 180.

    Eschenbach DA, Davick PR, Williams BL, Klebanoff SJ, Young-Smith K, Critchlow CM, Holmes KK. Prevalence of hydrogen peroxide-producing Lactobacillus species in normal women and women with bacterial vaginosis.. J Clin Microbiol. 1989;27(2):251–256. doi:.

    Not in our library10.1128/jcm.27.2.251-256.1989

  181. 181.

    Ocana VS, Pesce De Ruiz Holgado AA, Nader-Macias ME. Selection of vaginal H2O2-generating Lactobacillus species for probiotic use. Curr Microbiol. 1999;38(5):279–284. doi:.

    Not in our library10.1007/pl00006802

  182. 182.

    Ocana VS, De Ruiz Holgado AA, Nader-Macias ME. Growth inhibition of Staphylococcus aureus by H2O2-producing Lactobacillus paracasei subsp. paracasei isolated from the human vagina. FEMS Immunol Med Microbiol. 1999;23(2):87–92. doi:.

    Not in our library10.1016/s0928-8244(98)00116-3

  183. 183.

    Hawes SE, Hillier SL, Benedetti J, Stevens CE, Koutsky LA, Wolner- Hanssen P, Holmes KK. Hydrogen peroxide-producing lactobacilli and acquisition of vaginal infections. J Infect Dis. 1996;174(5):1058–1063. doi:.

    Not in our library10.1093/infdis/174.5.1058

  184. 184.

    Turroni F, Ventura M, Butto LF, Duranti S, O’Toole PW, Motherway MO, Sinderen D. Molecular dialogue between the human gut microbiota and the host: a Lactobacillus and Bifidobacterium perspective. Cell Mol Life Sci. 2014;71:183–203.

    Not in our library10.1007/s00018-013-1318-0

  185. 185.
    Siderophores in environmental research: roles and applications · 2014
    No notice
  186. 186.

    O’Sullivan DJ Isolated bifidobacteria that produce siderophores which inhibit growth of Lactococcus lactis. 2014. US patent 6746672B2.

    Not in our library

  187. 187.

    Vazquez-Gutierrez P, de Wouters T, Werder J, Chassard C, Lacroix C. High iron-sequestrating Bifidobacteria inhibit enteropathogen growth and adhesion to intestinal epithelial cells in vitro. Front Microbiol. 2016;7:1480. doi:.

    Not in our library10.3389/fmicb.2016.01480

  188. 188.

    Rodrigues L, Banat IM, Teixeira J, Oliveira R. Biosurfactants: potential applications in medicine. J Antimicrob Chemother. 2006;57(4):609–618. doi:.

    Not in our library10.1093/jac/dkl024

  189. 189.

    Saharan BS, Sahu RK, Sharma D. A review on biosurfactants: fermentation, current developments and perspectives. Genet Eng Biotechnol J. 2012;1:1–14.

    Not in our library

  190. 190.

    Rodrigues LR, Jeixeira JA, Van der Mei HC, Oliveira R. Physicochemical and functional characterization of a biosurfactant produced by Lactococcus lactis 53. Colloids and Surf B Biointerfaces. 2006;49(1):79–86. doi:.

    Not in our library10.1016/j.colsurfb.2006.03.003

  191. 191.

    Ciandrini E, Campana R, Casettari L, Perinelli DR, Faqioli L, Manti A, Palmieri GF, Papa S, Baffone W. Characterization of biosurfactants produced by Lactobacillus spp. and their activity against oral streptococci. Appl Microbiol Biotechnol. 2016;100(15):6767–6777. doi:.

    Not in our library10.1007/s00253-016-7531-7

  192. 192.

    Rodrigues LR, Teixeira JA, van der Mei HC, Oliveira R. Isolation and partial characterization of a biosurfactant produced by Streptococcus thermophilus A. Colloids Surf B Biointerfaces. 2006;53(1):105–112. doi:.

    Not in our library10.1016/j.colsurfb.2006.08.009

  193. 193.

    Saravanakumari P, Mani K. Structural characterization of a novel xylolipid biosurfactant from Lactococcus lactis and analysis of antibacterial activity against multi-drug resistant pathogens. Bioresour Technol. 2010;101(22):8851–8854. doi:.

    Not in our library10.1016/j.biortech.2010.06.104

  194. 194.

    Duarte C, Gudiña EJ, Lima CF, Rodrigues LR. Effects of biosurfactants on the viability and proliferation of human breast cancer cells. AMB Express. 2014;4(1):40. doi:.

    Not in our library10.1186/s13568-014-0040-0

  195. 195.

    Velraeds MM, Van Der Mei HC, Reid G, Busscher HJ. Inhibition of initial adhesion of uropathogenic Enterococcus faecalis by biosurfactants from Lactobacillus isolates. Appl Environ Microbiol. 1996;62(6):1958–1963. doi:.

    Not in our library10.1128/aem.62.6.1958-1963.1996

  196. 196.

    Reid G, Cook RL, Bruce AW. Examination of strains of lactobacilli for properties that may influence bacterial interference in the urinary tract. J Urol. 1987;138(2):330–335. doi:.

    Not in our library10.1016/s0022-5347(17)43137-5

  197. 197.

    Gomaa EZ. Antimicrobial and anti-adhesive properties of biosurfactant produced by lactobacilli isolates, biofilm formation and aggregation ability. J Gen Appl Microbiol. 2013;59(6):425–436. doi:.

    Not in our library10.2323/jgam.59.425

  198. 198.

    Sharma D, Saharan BS. Simultaneous production of biosurfactants and bacteriocins by probiotic Lactobacillus casei MRTL3. Int J Microbiol. 2014;2014:698713.

    Not in our library10.1155/2014/698713

  199. 199.

    Weinstein DL, O’Neill BL, Hone DM, Metcalf ES. Differential early interactions between Salmonella enterica serovar Typhimurium and two other pathogenic Salmonella serovars with intestinal epithelial cells. Infect Immun. 1998;66(5):2310–2318. doi:.

    Not in our library10.1128/iai.66.5.2310-2318.1998

  200. 200.

    Fujiwara S, Hashiba H, Hirota T, Forstner JF. Purification and characterization of a novel protein produced by Bifidobacterium longum SBT2928 that inhibits the binding of enterotoxigenic Escherichia coli Pb176 (CFA/II) to gangliotetraosylceramide. Appl Microbiol. 1999;86(4):615–621. doi:.

    Not in our library10.1046/j.1365-2672.1999.00705.x

  201. 201.

    Lievin V, Peiffer I, Hudault S, Rochat F, Brassart D, Neeser JR, Servin AL. Bifidobacterium strains from resident infant human gastrointestinal microflora exert antimicrobial activity. Gut. 2000;47(5):646–652. doi:.

    Not in our library10.1136/gut.47.5.646

  202. 202.

    Ohland CL, MacNaughton WK. Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol Gastrointest Liver Physiol. 2010;298(6):G807–G819. doi:.

    Not in our library10.1152/ajpgi.00243.2009

  203. 203.

    McGuckin MA, Eri R, Simms LA, Florin TH, Radford-Smith G. Intestinal barrier dysfunction in inflammatory bowel diseases. Inflam Bowel Dis. 2009;15(1):100–113. doi:.

    Not in our library10.1002/ibd.20539

  204. 204.

    Hooper LV, Macpherson AJ. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol. 2010;10(3):159–169. doi:.

    Not in our library10.1038/nri2710

  205. 205.

    Schneeberger EE, Lynch RD. The tight junction: a multifunctional complex. Am J Physiol Cell Physiol. 2004;286(6):C1213–C1228. doi:.

    Not in our library10.1152/ajpcell.00558.2003

  206. 206.

    Chichlowski M, Hale LP. Bacterial-mucosal interactions in inflammatory bowel disease - an alliance gone bad. Am J Physiol Gastrointest Liver Physiol. 2008;295(6):G1139–G1149. doi:.

    Not in our library10.1152/ajpgi.90516.2008

  207. 207.

    Sartor RB. Mechanisms of disease: pathogenesis of Crohn’s disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol. 2006;3(7):390–407. doi:.

    Not in our library10.1038/ncpgasthep0528

  208. 208.

    Moncada DM, Kammanadiminti SJ, Chadee K. Mucin and Toll-like receptors in host defence against intestinal parasites. Trends Parasitol. 2003;19(7):305–311. doi:.

    Not in our library10.1016/s1471-4922(03)00122-3

  209. 209.

    Corfield AP, Myerscough N, Longman R, Sylvester P, Arul S, Pignatelli M. Mucins and mucosal protection in the gastrointestinal tract: new prospects for mucins in the pathology of gastrointestinal disease. Gut. 2000;47(4):589–594. doi:.

    Not in our library10.1136/gut.47.4.589

  210. 210.

    Mattar AF, Teitelbaum DH, Drongowski RA, Yongyi F, Harmon CM, Coran AG. Probiotics up-regulate MUC-2 mucin gene expression in a Caco-2 cell-culture model. Pediatr Surg Int. 2002;18(7):586–590. doi:.

    Not in our library10.1007/s00383-002-0855-7

  211. 211.

    Mack DR, Michail S, Wei S, McDougall L, Hollingsworth MA. Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. Am J Physiol. 1999;276:G941–G950.

    Not in our library10.1152/ajpgi.1999.276.4.g941

  212. 212.

    Caballero-Franco C, Keller K, Simone C, Chadee K. The VSL#3 probiotic formula induces mucin gene expression and secretion in colonic epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2007;292(1):G315–G322. doi:.

    Not in our library10.1152/ajpgi.00265.2006

  213. 213.

    Reid G, McGroarty JA, Angotti R, Cook RL. Lactobacillus inhibitor production against Escherichia coli and coaggregation ability with uropathogens. Canadian J Microbiol. 1988;34(3):344–351. doi:.

    Not in our library10.1139/m88-063

  214. 214.

    Callado MC, Meriluoto J, Salminen S. Role of commercial probiotic strains against human pathogen adhesion to intestinal mucus. Lett Appl Microbiol. 2007;45:454–460.

    Not in our library10.1111/j.1472-765x.2007.02212.x

  215. 215.

    Kos B, Susković J, Vukovićm S, Simpraga M, Frece J, Matosić S. Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J Appl Microbiol. 2003;94(6):981–987. doi:.

    Not in our library10.1046/j.1365-2672.2003.01915.x

  216. 216.

    Kolenbrander PE. Oral microbial communities: biofilms, interactions, and genetic systems. Annu Rev Microbiol. 2000;54(1):413–439. doi:.

    Not in our library10.1146/annurev.micro.54.1.413

  217. 217.

    Mastromarino P, Brigidi P, Macchia S, Maggi L, Pirovano F, Trinchieri V, Conte U, Matteuzzi D. Characterization and selection of vaginal Lactobacillus strains for the preparation of vaginal tablets. J Appl Microbiol. 2002;93(5):884–893. doi:.

    Not in our library10.1046/j.1365-2672.2002.01759.x

  218. 218.

    Janković T, Frece J, Abram M, Gobin I. Aggregation ability of potential probiotic Lactobacillus plantarum strains. Int J Sanitary Eng Res. 2012;6:19–24.

    Not in our library

  219. 219.

    Schachtsiek M, Hammes WP, Hertel C. Characterization of Lactobacillus coryniformis DSM 20001T surface protein Cpf mediating coaggregation with and aggregation among pathogens. Appl Environ Microbiol. 2004;70(12):7078–7085. doi:.

    Not in our library10.1128/aem.70.12.7078-7085.2004

  220. 220.

    Mizuno K, Mizuno M, Yamauchi M, Takemura AJ, Romero VM, Morikawa K. Adjacent-possible ecological niche: growth of Lactobacillus species co-cultured with Escherichia coli in a synthetic minimal medium. Scient Rep. 2017;7(1):12880. doi:.

    Not in our library10.1038/s41598-017-12894-3

  221. 221.

    Spencer RJ, Chesson A. The effect of Lactobacillus spp. on the attachment of enterotoxigenic Escherichia coli to isolated porcine enterocytes. J Appl Bacteriol. 1994;77(2):215–220. doi:.

    Not in our library10.1111/j.1365-2672.1994.tb03066.x

  222. 222.

    Del Re B, Sgorbati B, Miglioli M, Palenzona D. Adhesion, autoaggregation and hydrophobicity of 13 strains of Bifidobacterium longum. Letters in Appl Microbiol. 2000;31(6):438–442. doi:.

    Not in our library10.1046/j.1365-2672.2000.00845.x

  223. 223.

    Boris S, Suárez JE, Barbés C. Characterization of the aggregation promoting factor from Lactobacillus gasseri, avaginal isolate. J Appl Microbiol. 1997;83(4):413–420. doi:.

    Not in our library10.1046/j.1365-2672.1997.00250.x

  224. 224.

    Sillanpää J, Martinez B, Antikainen J, Toba T, Kalkkinen N, Tankka S, Lounatmaa K, Keränen L, Höök M, Westerlund-Wikström B, et al. Characterization of the collagen-binding S-layer protein CbsA of Lactobacillus crispatus. J Bacteriol. 2000;182(22):6440–6450. doi:.

    Not in our library10.1128/jb.182.22.6440-6450.2000

  225. 225.

    Roos S, Lindgren S, Jonsson H. Autoaggregation of Lactobacillus reuteri is mediated by a putative DEAD-box helicase. Mol Microbiol. 1999;32(2):427–436. doi:.

    Not in our library10.1046/j.1365-2958.1999.01363.x

  226. 226.

    Jankovic I, Ventura M, Meylan V, Rouvet M, Elli M, Zink R. Contribution of aggregation-promoting factor to maintenance of cell shape in Lactobacillus gasseri 4B2. J Bacteriol. 2003;185(11):3288–3296. doi:.

    Not in our library10.1128/jb.185.11.3288-3296.2003

  227. 227.

    Reid G, Sobeli JD. Bacterial adherence in the pathogenesis of urinary tract infection: a review. Rev Infect Dis. 1987;9(3):470–487. doi:.

    Not in our library10.1093/clinids/9.3.470

  228. 228.

    Josenhans C, Suerbaum S. The role of motility as a virulence factor in bacteria. Int J Med Microbiol. 2002;291(8):605–614. doi:.

    Not in our library10.1078/1438-4221-00173

  229. 229.

    Stecher B, Hapfelmeier S, Müller C, Kremer M, Stallmach T, Hardt W. Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin-pretreated mice. Infect Immun. 2004;72(7):4138–4150. doi:.

    Not in our library10.1128/iai.72.7.4138-4150.2004

  230. 230.

    Dibb-Fuller MP, Allen-Vercoe E, Thorns CJ, Woodward MJ. Fimbriae- and flagella-mediated association with and invasion of cultured epithelial cells by Salmonella enteritidis. Microbiol. 1999;145(5):1023–1031. doi:.

    Not in our library10.1099/13500872-145-5-1023

  231. 231.

    Jones BD, Lee CA, Falkow S. Invasion by Salmonella typhimurium is affected by the direction of flagellar rotation.. Infect Immun. 1992;60(6):2475–2480. doi:.

    Not in our library10.1128/iai.60.6.2475-2480.1992

  232. 232.

    Schmitt CK, Ikeda JS, Darnell SC, Watson PR, Bispham J, Wallis TS, Weinstein DL, Metcalf ES, O’Brien AD. Absence of all components of the flagellar export and synthesis machinery differentially alters virulence of Salmonella enterica serovar Typhimurium in models of typhoid fever, survival in macrophages, tissue culture invasiveness, and calf enterocolitis. Infect Immun. 2001;69(9):5619–5625. doi:.

    Not in our library10.1128/iai.69.9.5619-5625.2001

  233. 233.

    Forbes SJ, Eschmann M, Mantis NJ. Inhibition of Salmonella enterica serovar Typhimurium motility and entry into epithelial cells by a protective antilipopolysaccharide monoclonal immunoglobulin a antibody. Infect Immun. 2008;76(9):4137–4144. doi:.

    Not in our library10.1128/iai.00416-08

  234. 234.

    Lièven-Le Moal V, Amsellem R, Servin AL. Impairment of swimming motility by antidiarrheic Lactobacillus acidophilus strain LB retards internalization of Salmonella enterica serovar Typhimurium within human enterocyte-like cells. Antimicrob Agents Chemother. 2011;55(10):4810–4820. doi:.

    Not in our library10.1128/aac.00418-11

  235. 235.

    Fayol-Messaoudi D, Coconier-Polter MH, Moal VL, Atassi F, Berger CN, Servin AL. The Lactobacillus plantarum strain ACADC287 isolated from a Greek cheese demonstrates antagonistic activity in vitro and in vivo against Salmonella enterica serovar Typhimurium. J Appl Microbiol. 2007;103(3):657–665. doi:.

    Not in our library10.1111/j.1365-2672.2007.03293.x

  236. 236.

    Yan F, Polk DB. Probiotics and immune health. Curr Opin Gastroenterol. 2011;27(6):496–501. doi:.

    Not in our library10.1097/mog.0b013e32834baa4d

  237. 237.

    Viaşu-Bolocan LV, Popescu F, Bica C. Probiotics and their immunomodulatory potential. Curr Health Sci J. 2013;39:204–209.

    Not in our library

  238. 238.

    Yan F, Polk DB. Probiotics: progress toward novel therapies for intestinal diseases. Curr Opin Gastroenterol. 2010;26(2):95–101. doi:.

    Not in our library10.1097/mog.0b013e328335239a

  239. 239.

    Meydani SN, Ha WK. Immunological effects of yoghurt. Am J Clin Nutr. 2000;71:861–872.

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    Lactobacillus amylovorus Inhibits the TLR4 Inflammatory Signaling Triggered by Enterotoxigenic Escherichia coli via Modulation of the Negative Regulators and Involvement of TLR2 in Intestinal Caco-2 Cells and Pig Explants · 2014
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