High-throughput mapping of the phage resistance landscape in E. coli

Abstract

Bacteriophages (phages) are critical players in the dynamics and function of microbial communities and drive processes as diverse as global biogeochemical cycles and human health. Phages tend to be predators finely tuned to attack specific hosts, even down to the strain level, which in turn defend themselves using an array of mechanisms. However, to date, efforts to rapidly and comprehensively identify bacterial host factors important in phage infection and resistance have yet to be fully realized. Here, we globally map the host genetic determinants involved in resistance to 14 phylogenetically diverse double-stranded DNA phages using two model Escherichia coli strains (K-12 and BL21) with known sequence divergence to demonstrate strain-specific differences. Using genome-wide loss-of-function and gain-of-function genetic technologies, we are able to confirm previously described phage receptors as well as uncover a number of previously unknown host factors that confer resistance to one or more of these phages. We uncover differences in resistance factors that strongly align with the susceptibility of K-12 and BL21 to specific phage. We also identify both phage-specific mechanisms, such as the unexpected role of cyclic-di-GMP in host sensitivity to phage N4, and more generic defenses, such as the overproduction of colanic acid capsular polysaccharide that defends against a wide array of phages. Our results indicate that host responses to phages can occur via diverse cellular mechanisms. Our systematic and high-throughput genetic workflow to characterize phage-host interaction determinants can be extended to diverse bacteria to generate datasets that allow predictive models of how phage-mediated selection will shape bacterial phenotype and evolution. The results of this study and future efforts to map the phage resistance landscape will lead to new insights into the coevolution of hosts and their phage, which can ultimately be used to design better phage therapeutic treatments and tools for precision microbiome engineering.

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     Karow M, Raina S, Georgopoulos C, Fayet O. Complex phenotypes of null mutations in the htr genes, whose products are essential for Escherichia coli growth at elevated temperatures. Res Microbiol. 1991;142: 289–294.

     Not in our library10.1016/0923-2508(91)90043-a

112. 112.

     Pagnout C, Sohm B, Razafitianamaharavo A, Caillet C, Offroy M, Leduc M, et al Pleiotropic effects of rfa-gene mutations on Escherichia coli envelope properties. Sci Rep. 2019;9: 9696

     Not in our library10.1038/s41598-019-46100-3

113. 113.

     Klein G, Raina S. Regulated Assembly of LPS, Its Structural Alterations and Cellular Response to LPS Defects. Int J Mol Sci. 2019;20

     Not in our library10.3390/ijms20020356

114. 114.

     Mitchell AM, Silhavy TJ. Envelope stress responses: balancing damage repair and toxicity. Nat Rev Microbiol. 2019;17: 417–428.

     Not in our library10.1038/s41579-019-0199-0

115. 115.

     Meaden S, Paszkiewicz K, Koskella B. The cost of phage resistance in a plant pathogenic bacterium is context‐dependent. Evolution. 2015:1321–1328.

     Not in our library10.1111/evo.12652

116. 116.

     Díaz-Muñoz SL, Koskella B. Bacteria–Phage Interactions in Natural Environments. Advances in Applied Microbiology. 2014:135–183.

     Not in our library10.1016/b978-0-12-800259-9.00004-4

117. 117.

     Mirzaei MK, Maurice CF. Ménage à trois in the human gut: interactions between host, bacteria and phages. Nature Reviews Microbiology. 2017:397–408.

     Not in our library10.1038/nrmicro.2017.30

118. 118.

     Padfield D, Castledine M, Buckling A. Temperature-dependent changes to host-parasite interactions alter the thermal performance of a bacterial host. ISME J. 2020;14: 389–398.

     Not in our library10.1038/s41396-019-0526-5

119. 119.

     Alseth EO, Pursey E, Luján AM, McLeod I, Rollie C, Westra ER. Bacterial biodiversity drives the evolution of CRISPR-based phage resistance. Nature. 2019;574: 549–552.

     Not in our library10.1038/s41586-019-1662-9

120. 120.

     Kortright KE, Chan BK, Turner PE. High-throughput discovery of phage receptors using transposon insertion sequencing of bacteria. Proc Natl Acad Sci U S A. 2020

     Not in our library10.1073/pnas.2001888117

121. 121.

     Shibuya I. Metabolic regulations and biological functions of phospholipids in Escherichia coli. Prog Lipid Res. 1992;31: 245–299.

     Not in our library10.1016/0163-7827(92)90010-g

122. 122.

     Dalebroux ZD, Edrozo MB, Pfuetzner RA, Ressl S, Kulasekara BR, Blanc M-P, et al Delivery of cardiolipins to the Salmonella outer membrane is necessary for survival within host tissues and virulence. Cell Host Microbe. 2015;17: 441–451.

     Not in our library10.1016/j.chom.2015.03.003

123. 123.

     Nepper JF, Lin YC, Weibel DB. Rcs phosphorelay activation in cardiolipin-deficient Escherichia coli reduces biofilm formation. J Bacteriol. 2019: 201(9): e00804–18.

     Not in our library10.1128/jb.00804-18

124. 124.

     Zhou Y, Filter JJ, Court DL, Gottesman ME, Friedman DI. Requirement for NusG for transcription antitermination in vivo by the lambda N protein. J Bacteriol. 2002;184: 3416–3418.

     Not in our library10.1128/jb.184.12.3416-3418.2002

125. 125.

     Sullivan SL, Gottesman ME. Requirement for E. coli NusG protein in factor-dependent transcription termination. Cell. 1992;68: 989–994.

     Not in our library10.1016/0092-8674(92)90041-a

126. 126.

     Henthorn KS. Multilevel regulation of gene expression in lambda and related bacteriophages [thesis]. University of Michigan; 1994. http://hdl.handle.net/2027.42/103954.

     Not in our library

127. 127.

     Bertani B, Ruiz N. Function and Biogenesis of Lipopolysaccharides. EcoSal Plus. 2018;8

     Not in our library10.1128/ecosalplus.esp-0001-2018

128. 128.

     Konovalova A, Kahne DE, Silhavy TJ. Outer Membrane Biogenesis. Annu Rev Microbiol. 2017;71: 539–556.

     Not in our library10.1146/annurev-micro-090816-093754

129. 129.
     Global role of the bacterial post-transcriptional regulator CsrA revealed by integrated transcriptomics · 2017

     No notice
130. 130.

     Romeo T, Babitzke P. Global Regulation by CsrA and Its RNA Antagonists. Microbiol Spectr. 2018;6

     Not in our library10.1128/microbiolspec.rwr-0009-2017

131. 131.

     Mojardín L, Salas M. Global Transcriptional Analysis of Virus-Host Interactions between Phage ϕ29 and Bacillus subtilis. Journal of Virology. 2016:9293–9304.

     Not in our library10.1128/jvi.01245-16

132. 132.

     Chevallereau A, Blasdel BG, De Smet J, Monot M, Zimmermann M, Kogadeeva M, et al Next-Generation “-omics” Approaches Reveal a Massive Alteration of Host RNA Metabolism during Bacteriophage Infection of Pseudomonas aeruginosa. PLoS Genet. 2016;12: e1006134

     Not in our library10.1371/journal.pgen.1006134

133. 133.

     Hantke K. Major outer membrane proteins of E. coli K12 serve as receptors for the phages T2 (protein Ia) and 434 (protein Ib). Molecular and General Genetics MGG. 1978:131–135.

     Not in our library10.1007/bf00267377

134. 134.

     Grigonyte AM, Harrison C, MacDonald PR, Montero-Blay A, Tridgett M, Duncan J, et al Comparison of CRISPR and Marker-Based Methods for the Engineering of Phage T7. Viruses. 2020;12

     Not in our library10.3390/v12020193

135. 135.

     Prelich G. Gene overexpression: uses, mechanisms, and interpretation. Genetics. 2012;190: 841–854.

     Not in our library10.1534/genetics.111.136911

136. 136.

     Veitia RA, Bottani S, Birchler JA. Gene dosage effects: nonlinearities, genetic interactions, and dosage compensation. Trends Genet. 2013;29: 385–393.

     Not in our library10.1016/j.tig.2013.04.004

137. 137.

     van Leeuwen J, Pons C, Boone C, Andrews BJ. Mechanisms of suppression: The wiring of genetic resilience. Bioessays. 2017;39

     Not in our library10.1002/bies.201700042

138. 138.

     Holzmayer TA, Pestov DG, Roninson IB. Isolation of dominant negative mutants and inhibitory antisense RNA sequences by expression selection of random DNA fragments. Nucleic Acids Res. 1992;20: 711–717.

     Not in our library10.1093/nar/20.4.711

139. 139.

     Sopko R, Huang D, Preston N, Chua G, Papp B, Kafadar K, et al Mapping pathways and phenotypes by systematic gene overexpression. Mol Cell. 2006;21: 319–330.

     Not in our library10.1016/j.molcel.2005.12.011

140. 140.

     Cardarelli L, Maxwell KL, Davidson AR. Assembly mechanism is the key determinant of the dosage sensitivity of a phage structural protein. Proc Natl Acad Sci U S A. 2011;108: 10168–10173.

     Not in our library10.1073/pnas.1100759108

141. 141.

     Plumbridge J. Control of the expression of the manXYZ operon in Escherichia coli: Mlc is a negative regulator of the mannose PTS. Mol Microbiol. 1998;27: 369–380.

     Not in our library10.1046/j.1365-2958.1998.00685.x

142. 142.

     Decker K, Plumbridge J, Boos W. Negative transcriptional regulation of a positive regulator: the expression of malT, encoding the transcriptional activator of the maltose regulon of Escherichia coli, is negatively controlled by Mlc. Mol Microbiol. 1998;27: 381–390.

     Not in our library10.1046/j.1365-2958.1998.00694.x

143. 143.

     Joly N, Danot O, Schlegel A, Boos W, Richet E. The Aes protein directly controls the activity of MalT, the central transcriptional activator of the Escherichia coli maltose regulon. J Biol Chem. 2002;277: 16606–16613.

     Not in our library10.1074/jbc.m200991200

144. 144.

     Lee SJ, Boos W, Bouché JP, Plumbridge J. Signal transduction between a membrane-bound transporter, PtsG, and a soluble transcription factor, Mlc, of Escherichia coli. EMBO J. 2000;19: 5353–5361.

     Not in our library10.1093/emboj/19.20.5353

145. 145.

     Schlegel A, Danot O, Richet E, Ferenci T, Boos W. The N Terminus of the Escherichia coli Transcription Activator MalT Is the Domain of Interaction with MalY. Journal of Bacteriology. 2002:3069–3077.

     Not in our library10.1128/jb.184.11.3069-3077.2002

146. 146.

     Reidl J, Boos W. The malX malY operon of Escherichia coli encodes a novel enzyme II of the phosphotransferase system recognizing glucose and maltose and an enzyme abolishing the endogenous induction of the maltose system. J Bacteriol. 1991;173: 4862–4876.

     Not in our library10.1128/jb.173.15.4862-4876.1991

147. 147.

     Lengsfeld C, Schönert S, Dippel R, Boos W. Glucose- and glucokinase-controlled mal gene expression in Escherichia coli. J Bacteriol. 2009;191: 701–712.

     Not in our library10.1128/jb.00767-08

148. 148.

     Hong JS, Smith GR, Ames BN. Adenosine 3’:5’-cyclic monophosphate concentration in the bacterial host regulates the viral decision between lysogeny and lysis. Proc Natl Acad Sci U S A. 1971;68: 2258–2262.

     Not in our library10.1073/pnas.68.9.2258

149. 149.

     Grodzicker T, Arditti RR, Eisen H. Establishment of repression by lambdoid phage in catabolite activator protein and adenylate cyclase mutants of Escherichia coli. Proc Natl Acad Sci U S A. 1972;69: 366–370.

     Not in our library10.1073/pnas.69.2.366

150. 150.

     Jenal U, Reinders A, Lori C. Cyclic di-GMP: second messenger extraordinaire. Nat Rev Microbiol. 2017;15: 271–284.

     Not in our library10.1038/nrmicro.2016.190

151. 151.

     Römling U, Galperin MY, Gomelsky M. Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev. 2013;77: 1–52.

     Not in our library10.1128/mmbr.00043-12

152. 152.

     Hengge R. Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol. 2009;7: 263–273.

     Not in our library10.1038/nrmicro2109

153. 153.

     Hall BG. The rtn gene of Proteus vulgaris is actually from Escherichia coli. Journal of Bacteriology. 1997:2433–2434.

     Not in our library10.1128/jb.179.7.2433-2434.1997

154. 154.

     Chae KS, Yoo OJ. Cloning of the lambda resistant genes from Brevibacterium albidum and Proteus vulgaris into Escherichia coli. Biochem Biophys Res Commun. 1986;140: 1101–1105.

     Not in our library10.1016/0006-291x(86)90748-5

155. 155.

     Norioka S, Ramakrishnan G, Ikenaka K, Inouye M. Interaction of a transcriptional activator, OmpR, with reciprocally osmoregulated genes, ompF and ompC, of Escherichia coli. J Biol Chem. 1986;261: 17113–17119.

     Not in our library

156. 156.

     Yoshida T, Qin L, Egger LA, Inouye M. Transcription regulation of ompF and ompC by a single transcription factor, OmpR. J Biol Chem. 2006;281: 17114–17123.

     Not in our library10.1074/jbc.m602112200

157. 157.

     Mizuno T, Mizushima S. Signal transduction and gene regulation through the phosphorylation of two regulatory components: the molecular basis for the osmotic regulation of the porin genes. Mol Microbiol. 1990;4: 1077–1082.

     Not in our library10.1111/j.1365-2958.1990.tb00681.x

158. 158.

     Andersen J, Forst SA, Zhao K, Inouye M, Delihas N. The function of micF RNA. micF RNA is a major factor in the thermal regulation of OmpF protein in Escherichia coli. J Biol Chem. 1989;264: 17961–17970.

     Not in our library

159. 159.

     Deighan P, Free A, Dorman CJ. A role for the Escherichia coli H-NS-like protein StpA in OmpF porin expression through modulation of micF RNA stability. Mol Microbiol. 2000;38: 126–139.

     Not in our library10.1046/j.1365-2958.2000.02120.x

160. 160.

     Kao C, Snyder L. The lit gene product which blocks bacteriophage T4 late gene expression is a membrane protein encoded by a cryptic DNA element, e14. J Bacteriol. 1988;170: 2056–2062.

     Not in our library10.1128/jb.170.5.2056-2062.1988

161. 161.

     Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, Toyonaga H, et al Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res. 2005;12: 291–299.

     Not in our library10.1093/dnares/dsi012

162. 162.

     Cano DA, Domínguez-Bernal G, Tierrez A, Garcia-Del Portillo F, Casadesús J. Regulation of capsule synthesis and cell motility in Salmonella enterica by the essential gene igaA. Genetics. 2002;162: 1513–1523.

     Not in our library10.1093/genetics/162.4.1513

163. 163.

     Cho S-H, Szewczyk J, Pesavento C, Zietek M, Banzhaf M, Roszczenko P, et al Detecting envelope stress by monitoring β-barrel assembly. Cell. 2014;159: 1652–1664.

     Not in our library10.1016/j.cell.2014.11.045

164. 164.

     Stevenson G, Andrianopoulos K, Hobbs M, Reeves PR. Organization of the Escherichia coli K-12 gene cluster responsible for production of the extracellular polysaccharide colanic acid. Journal of bacteriology. 1996:4885–4893.

     Not in our library10.1128/jb.178.16.4885-4893.1996

165. 165.

     Hussein NA, Cho S-H, Laloux G, Siam R, Collet J-F. Distinct domains of Escherichia coli IgaA connect envelope stress sensing and down-regulation of the Rcs phosphorelay across subcellular compartments. PLoS Genet. 2018;14: e1007398

     Not in our library10.1371/journal.pgen.1007398

166. 166.

     Majdalani N, Gottesman S. The Rcs phosphorelay: a complex signal transduction system. Annu Rev Microbiol. 2005;59: 379–405.

     Not in our library10.1146/annurev.micro.59.050405.101230

167. 167.

     Chaudhry W, Lee E, Worthy A, Weiss Z, Grabowicz M, Vega N, et al Mucoidy, a general mechanism for maintaining lytic phage in populations of bacteria. FEMS Microbiology Ecology. 2020

     Not in our library10.1093/femsec/fiaa162

168. 168.

     Scanlan PD, Buckling A. Co-evolution with lytic phage selects for the mucoid phenotype of Pseudomonas fluorescens SBW25. ISME J. 2012;6: 1148–1158.

     Not in our library10.1038/ismej.2011.174

169. 169.

     Martin DR. Mucoid Variation in Pseudomonas AeruginosaInduced by the Action of Phage. Journal of Medical Microbiology. 1973:111–118.

     Not in our library10.1099/00222615-6-1-111

170. 170.

     Mizoguchi K, Morita M, Fischer CR, Yoichi M, Tanji Y, Unno H. Coevolution of bacteriophage PP01 and Escherichia coli O157:H7 in continuous culture. Appl Environ Microbiol. 2003;69: 170–176.

     Not in our library10.1128/aem.69.1.170-176.2003

171. 171.

     Keseler IM, Mackie A, Santos-Zavaleta A, Billington R, Bonavides-Martínez C, Caspi R, et al The EcoCyc database: reflecting new knowledge about Escherichia coli K-12. Nucleic Acids Res. 2017;45: D543–D550.

     Not in our library10.1093/nar/gkw1003

172. 172.

     Reinders A, Hee C-S, Ozaki S, Mazur A, Boehm A, Schirmer T, et al Expression and Genetic Activation of Cyclic Di-GMP-Specific Phosphodiesterases in Escherichia coli. J Bacteriol. 2016;198: 448–462.

     Not in our library10.1128/jb.00604-15

173. 173.

     Hengge R, Galperin MY, Ghigo J-M, Gomelsky M, Green J, Hughes KT, et al Systematic Nomenclature for GGDEF and EAL Domain-Containing Cyclic Di-GMP Turnover Proteins of Escherichia coli. J Bacteriol. 2016;198: 7–11.

     Not in our library10.1128/jb.00424-15

174. 174.

     Povolotsky TL, Hengge R. Genome-Based Comparison of Cyclic Di-GMP Signaling in Pathogenic and Commensal Escherichia coli Strains. J Bacteriol. 2016;198: 111–126.

     Not in our library10.1128/jb.00520-15

175. 175.

     Park JH, Lee KH, Kim TY, Lee SY. Metabolic engineering of Escherichia coli for the production of L-valine based on transcriptome analysis and in silico gene knockout simulation. Proc Natl Acad Sci U S A. 2007;104: 7797–7802.

     Not in our library10.1073/pnas.0702609104

176. 176.

     Lehnen D, Blumer C, Polen T, Wackwitz B, Wendisch VF, Unden G. LrhA as a new transcriptional key regulator of flagella, motility and chemotaxis genes in Escherichia coli. Mol Microbiol. 2002;45: 521–532.

     Not in our library10.1046/j.1365-2958.2002.03032.x

177. 177.

     Göpel Y, Khan MA, Görke B. Ménage à trois: post-transcriptional control of the key enzyme for cell envelope synthesis by a base-pairing small RNA, an RNase adaptor protein, and a small RNA mimic. RNA Biol. 2014;11: 433–442.

     Not in our library10.4161/rna.28301

178. 178.

     McPartland J, Rothman-Denes LB. The tail sheath of bacteriophage N4 interacts with the Escherichia coli receptor. J Bacteriol. 2009;191: 525–532.

     Not in our library10.1128/jb.01423-08

179. 179.
     Characterization of the interactions between Escherichia coli receptors, LPS and OmpC, and bacteriophage T4 long tail fibers · 2016

     No notice
180. 180.

     Hattman S, Fukasawa T. HOST-INDUCED MODIFICATION OF T-EVEN PHAGES DUE TO DEFECTIVE GLUCOSYLATION OF THEIR DNA. Proc Natl Acad Sci U S A. 1963;50: 297–300.

     Not in our library10.1073/pnas.50.2.297

181. 181.

     Prehm P, Jann B, Jann K, Schmidt G, Stirm S. On a bacteriophage T3 and T4 receptor region within the cell wall lipopolysaccharide of escherichia coli B. J Mol Biol. 1976;101: 277–281.

     Not in our library10.1016/0022-2836(76)90377-6

182. 182.

     Lenski RE. Two-step resistance by Escherichia coli B to bacteriophage T2. Genetics. 1984;107: 1–7.

     Not in our library10.1093/genetics/107.1.1

183. 183.

     Boos W, Shuman H. Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation. Microbiol Mol Biol Rev. 1998;62: 204–229.

     Not in our library10.1128/mmbr.62.1.204-229.1998

184. 184.

     Plumbridge J. Control of the expression of the manXYZ operon in Escherichia coli: Mlc is a negative regulator of the mannose PTS. Mol Microbiol. 1998;27: 369–380.

     Not in our library10.1046/j.1365-2958.1998.00685.x

185. 185.

     Decker K, Plumbridge J, Boos W. Negative transcriptional regulation of a positive regulator: the expression of malT, encoding the transcriptional activator of the maltose regulon of Escherichia coli, is negatively controlled by Mlc. Mol Microbiol. 1998;27: 381–390.

     Not in our library10.1046/j.1365-2958.1998.00694.x

186. 186.

     Lee SJ, Boos W, Bouché JP, Plumbridge J. Signal transduction between a membrane-bound transporter, PtsG, and a soluble transcription factor, Mlc, of Escherichia coli. EMBO J. 2000;19: 5353–5361.

     Not in our library10.1093/emboj/19.20.5353

187. 187.

     Lee SJ, Boos W, Bouché JP, Plumbridge J. Signal transduction between a membrane-bound transporter, PtsG, and a soluble transcription factor, Mlc, of Escherichia coli. EMBO J. 2000;19: 5353–5361.

     Not in our library10.1093/emboj/19.20.5353

188. 188.

     Danese PN, Pratt LA, Kolter R. Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J Bacteriol. 2000;182: 3593–3596.

     Not in our library10.1128/jb.182.12.3593-3596.2000

189. 189.

     Eydallin G, Morán-Zorzano MT, Muñoz FJ, Baroja-Fernández E, Montero M, Alonso-Casajús N, et al An Escherichia coli mutant producing a truncated inactive form of GlgC synthesizes glycogen: further evidences for the occurrence of various important sources of ADPglucose in enterobacteria. FEBS Lett. 2007;581: 4417–4422.

     Not in our library10.1016/j.febslet.2007.08.016

190. 190.

     Baker CS, Morozov I, Suzuki K, Romeo T, Babitzke P. CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli. Mol Microbiol. 2002;44: 1599–1610.

     Not in our library10.1046/j.1365-2958.2002.02982.x

191. 191.

     Romeo T, Gong M, Liu MY, Brun-Zinkernagel AM. Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J Bacteriol. 1993;175: 4744–4755.

     Not in our library10.1128/jb.175.15.4744-4755.1993

192. 192.

     Wang X, Dubey AK, Suzuki K, Baker CS, Babitzke P, Romeo T. CsrA post-transcriptionally represses pgaABCD, responsible for synthesis of a biofilm polysaccharide adhesin of Escherichia coli. Mol Microbiol. 2005;56: 1648–1663.

     Not in our library10.1111/j.1365-2958.2005.04648.x

193. 193.

     Jackson DW, Suzuki K, Oakford L, Simecka JW, Hart ME, Romeo T. Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J Bacteriol. 2002;184: 290–301.

     Not in our library10.1128/jb.184.1.290-301.2002

194. 194.

     Palaniyandi S, Mitra A, Herren CD, Lockatell CV, Johnson DE, Zhu X, et al BarA-UvrY two-component system regulates virulence of uropathogenic E. coli CFT073. PLoS ONE. 2012;7: e31348

     Not in our library10.1371/journal.pone.0031348

195. 195.

     Klein G, Raina S. Regulated Control of the Assembly and Diversity of LPS by Noncoding sRNAs. Biomed Res Int. 2015;2015: 153561

     Not in our library10.1155/2015/153561

196. 196.

     Murata A, Odaka M, Mukuno S. The Bacteriophage-Inactivating Effect of Basic Amino Acids; Arginine, Histidine, and Lysine. Agric Biol Chem. 1974;38: 477–478.

     Not in our library

197. 197.

     Lau CKY, Krewulak KD, Vogel HJ. Bacterial ferrous iron transport: the Feo system. FEMS Microbiol Rev. 2016;40: 273–298.

     Not in our library10.1093/femsre/fuv049

198. 198.

     Kammler M, Schön C, Hantke K. Characterization of the ferrous iron uptake system of Escherichia coli. J Bacteriol. 1993;175: 6212–6219.

     Not in our library10.1128/jb.175.19.6212-6219.1993

199. 199.

     Hantke K. Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol Gen Genet. 1981;182: 288–292.

     Not in our library10.1007/bf00269672

200. 200.

     Carpenter BM, Whitmire JM, Merrell DS. This Is Not Your Mother’s Repressor: the Complex Role of Fur in Pathogenesis. Infection and Immunity. 2009 pp. 2590–2601.

     Not in our library10.1128/iai.00116-09

201. 201.

     Braun V. FhuA (TonA), the career of a protein. J Bacteriol. 2009;191: 3431–3436.

     Not in our library10.1128/jb.00106-09

202. 202.

     Heinrichs DE, Yethon JA, Whitfield C. Molecular basis for structural diversity in the core regions of the lipopolysaccharides of Escherichia coli and Salmonella enterica. Mol Microbiol. 1998;30: 221–232.

     Not in our library10.1046/j.1365-2958.1998.01063.x

203. 203.

     Ornellas EP, Stocker BA. Relation of lipopolysaccharide character to P1 sensitivity in Salmonella typhimurium. Virology. 1974;60: 491–502.

     Not in our library10.1016/0042-6822(74)90343-2

204. 204.

     Ho TD, Waldor MK. Enterohemorrhagic Escherichia coli O157:H7 gal mutants are sensitive to bacteriophage P1 and defective in intestinal colonization. Infect Immun. 2007;75: 1661–1666.

     Not in our library10.1128/iai.01342-06

205. 205.

     Raetz CRH, Whitfield C. Lipopolysaccharide Endotoxins. Annual Review of Biochemistry. 2002 pp. 635–700.

     Not in our library10.1146/annurev.biochem.71.110601.135414

206. 206.

     Nikaido H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev. 2003;67: 593–656.

     Not in our library10.1128/mmbr.67.4.593-656.2003

207. 207.

     Thibault D, Jensen PA, Wood S, Qabar C, Clark S, Shainheit MG, et al Droplet Tn-Seq combines microfluidics with Tn-Seq for identifying complex single-cell phenotypes. Nat Commun. 2019;10: 5729

     Not in our library10.1038/s41467-019-13719-9

208. 208.

     Hernandez CA, Koskella B. Phage resistance evolution in vitro is not reflective of in vivo outcome in a plant-bacteria-phage system. Evolution. 2019;73: 2461–2475.

     Not in our library10.1111/evo.13833

209. 209.

     Qimron U, Kulczyk AW, Hamdan SM, Tabor S, Richardson CC. Inadequate inhibition of host RNA polymerase restricts T7 bacteriophage growth on hosts overexpressing udk. Mol Microbiol. 2008;67: 448–457.

     Not in our library10.1111/j.1365-2958.2007.06058.x

210. 210.
     Magic Pools: Parallel Assessment of Transposon Delivery Vectors in Bacteria · 2018

     Not checked
211. 211.

     Nora LC, Westmann CA, Guazzaroni M-E, Siddaiah C, Gupta VK, Silva-Rocha R. Recent advances in plasmid-based tools for establishing novel microbial chassis. Biotechnol Adv. 2019;37: 107433

     Not in our library10.1016/j.biotechadv.2019.107433

212. 212.
     Resistance Development to Bacteriophages Occurring during Bacteriophage Therapy · 2018

     No notice
213. 213.

     Abedon ST. Bacteriophage Ecology: Population Growth, Evolution, and Impact of Bacterial Viruses. Cambridge University Press; 2008.

     Not in our library

214. 214.

     Díaz-Muñoz SL, Koskella B. Bacteria-phage interactions in natural environments. Adv Appl Microbiol. 2014;89: 135–183.

     Not in our library10.1016/b978-0-12-800259-9.00004-4

215. 215.

     Oechslin F, Piccardi P, Mancini S, Gabard J, Moreillon P, Entenza JM, et al Synergistic Interaction Between Phage Therapy and Antibiotics Clears Pseudomonas Aeruginosa Infection in Endocarditis and Reduces Virulence. J Infect Dis. 2017;215: 703–712.

     Not in our library10.1093/infdis/jiw632

216. 216.

     Hung C-H, Kuo C-F, Wang C-H, Wu C-M, Tsao N. Experimental phage therapy in treating Klebsiella pneumoniae-mediated liver abscesses and bacteremia in mice. Antimicrob Agents Chemother. 2011;55: 1358–1365.

     Not in our library10.1128/aac.01123-10

217. 217.

     Taylor VL, Fitzpatrick AD, Islam Z, Maxwell KL. The Diverse Impacts of Phage Morons on Bacterial Fitness and Virulence. Adv Virus Res. 2019;103: 1–31.

     Not in our library10.1016/bs.aivir.2018.08.001

218. 218.
     Bacteria–phage coevolution as a driver of ecological and evolutionary processes in microbial communities · 2014

     No notice
219. 219.

     Castillo D, Rørbo N, Jørgensen J, Lange J, Tan D, Kalatzis PG, et al Phage defense mechanisms and their genomic and phenotypic implications in the fish pathogen Vibrio anguillarum. FEMS Microbiol Ecol. 2019;95

     Not in our library10.1093/femsec/fiz004

220. 220.

     Wang X, Wei Z, Yang K, Wang J, Jousset A, Xu Y, et al Phage combination therapies for bacterial wilt disease in tomato. Nat Biotechnol. 2019;37: 1513–1520.

     Not in our library10.1038/s41587-019-0328-3

221. 221.

     McCallin S, Oechslin F. Bacterial Resistance to Phage and Its Impact on Clinical Therapy In: Phage Therapy: A Practical Approach. Springer Nature Switzerland AG; 2019 pp. 59–88.

     Not in our library

222. 222.

     Pires DP, Cleto S, Sillankorva S, Azeredo J, Lu TK. Genetically Engineered Phages: a Review of Advances over the Last Decade. Microbiol Mol Biol Rev. 2016;80: 523–543.

     Not in our library10.1128/mmbr.00069-15

223. 223.

     Kilcher S, Loessner MJ. Engineering Bacteriophages as Versatile Biologics. Trends Microbiol. 2019;27: 355–367.

     Not in our library10.1016/j.tim.2018.09.006

224. 224.

     Ando H, Lemire S, Pires DP, Lu TK. Engineering Modular Viral Scaffolds for Targeted Bacterial Population Editing. Cell Syst. 2015;1: 187–196.

     Not in our library10.1016/j.cels.2015.08.013

225. 225.

     Chan BK, Abedon ST, Loc-Carrillo C. Phage cocktails and the future of phage therapy. Future Microbiol. 2013;8: 769–783.

     Not in our library10.2217/fmb.13.47

226. 226.

     Yehl K, Lemire S, Yang AC, Ando H, Mimee M, Torres MDT, et al Engineering Phage Host-Range and Suppressing Bacterial Resistance through Phage Tail Fiber Mutagenesis. Cell. 2019;179: 459–469.e9.

     Not in our library10.1016/j.cell.2019.09.015

227. 227.

     Yosef I, Goren MG, Globus R, Molshanski-Mor S, Qimron U. Extending the Host Range of Bacteriophage Particles for DNA Transduction. Mol Cell. 2017;66: 721–728.e3.

     Not in our library10.1016/j.molcel.2017.04.025

228. 228.

     Yosef I, Manor M, Kiro R, Qimron U. Temperate and lytic bacteriophages programmed to sensitize and kill antibiotic-resistant bacteria. Proc Natl Acad Sci U S A. 2015;112: 7267–7272.

     Not in our library10.1073/pnas.1500107112

229. 229.
     Resistance Evolution against Phage Combinations Depends on the Timing and Order of Exposure · 2019

     No notice
230. 230.

     Kilcher S, Studer P, Muessner C, Klumpp J, Loessner MJ. Cross-genus rebooting of custom-made, synthetic bacteriophage genomes in L-form bacteria. Proc Natl Acad Sci U S A. 2018;115: 567–572.

     Not in our library10.1073/pnas.1714658115

231. 231.

     Kutter E, Sulakvelidze A. Bacteriophages: Biology and Applications. CRC Press; 2004.

     Not in our library

232. 232.

     Dunne M, Rupf B, Tala M, Qabrati X, Ernst P, Shen Y, et al Reprogramming Bacteriophage Host Range through Structure-Guided Design of Chimeric Receptor Binding Proteins. Cell Rep. 2019;29: 1336–1350.e4.

     Not in our library10.1016/j.celrep.2019.09.062

233. 233.

     Nobrega FL, Costa AR, Kluskens LD, Azeredo J. Revisiting phage therapy: new applications for old resources. Trends in Microbiology. 2015:185–191.

     Not in our library10.1016/j.tim.2015.01.006

234. 234.

     Sturino JM, Klaenhammer TR. Engineered bacteriophage-defence systems in bioprocessing. Nat Rev Microbiol. 2006;4: 395–404.

     Not in our library10.1038/nrmicro1393

235. 235.

     Mahony J, Ainsworth S, Stockdale S, van Sinderen D. Phages of lactic acid bacteria: The role of genetics in understanding phage-host interactions and their co-evolutionary processes. Virology. 2012:143–150.

     Not in our library10.1016/j.virol.2012.10.008

236. 236.

     Ma NJ, Isaacs FJ. Genomic Recoding Broadly Obstructs the Propagation of Horizontally Transferred Genetic Elements. Cell Syst. 2016;3: 199–207.

     Not in our library10.1016/j.cels.2016.06.009

237. 237.

     Lajoie MJ, Rovner AJ, Goodman DB, Aerni H-R, Haimovich AD, Kuznetsov G, et al Genomically recoded organisms expand biological functions. Science. 2013;342: 357–360.

     Not in our library10.1126/science.1241459

238. 238.

     Spears PA, Mitsu Suyemoto M, Hamrick TS, Wolf RL, Havell EA, Orndorff PE. In VitroProperties of a Listeria monocytogenes Bacteriophage-Resistant Mutant Predict Its Efficacy as a Live Oral Vaccine Strain. Infection and Immunity. 2011:5001–5009.

     Not in our library10.1128/iai.05700-11

239. 239.

     Capparelli R, Nocerino N, Lanzetta R, Silipo A, Amoresano A, Giangrande C, et al Bacteriophage-resistant Staphylococcus aureus mutant confers broad immunity against staphylococcal infection in mice. PLoS ONE. 2010;5: e11720

     Not in our library10.1371/journal.pone.0011720

240. 240.

     Capparelli R, Nocerino N, Iannaccone M, Ercolini D, Parlato M, Chiara M, et al Bacteriophage therapy of Salmonella enterica: a fresh appraisal of bacteriophage therapy. J Infect Dis. 2010;201: 52–61.

     Not in our library10.1086/648478

241. 241.

     Dąbrowska K, Abedon ST. Pharmacologically Aware Phage Therapy: Pharmacodynamic and Pharmacokinetic Obstacles to Phage Antibacterial Action in Animal and Human Bodies. Microbiol Mol Biol Rev. 2019;83

     Not in our library10.1128/mmbr.00012-19

242. 242.

     Adler BA, Zhong C, Liu H, Kutter E, Deutschbauer AM, Mutalik VK, et al Systematic Discovery of Salmonella Phage-Host Interactions via High-Throughput Genome-Wide Screens. bioRxiv [Preprint]. 2020 [cited 2020 Mar 10]

     Not in our library10.1101/2020.04.27.058388

243. 243.
     Fitness Trade-Offs Resulting from Bacteriophage Resistance Potentiate Synergistic Antibacterial Strategies · 2020

     No notice
244. 244.

     Torres-Barceló C, Hochberg ME. Evolutionary Rationale for Phages as Complements of Antibiotics. Trends Microbiol. 2016;24: 249–256.

     Not in our library10.1016/j.tim.2015.12.011

245. 245.
     Fighting Pathogenic Bacteria on Two Fronts: Phages and Antibiotics as Combined Strategy · 2019

     No notice
246. 246.
     Phage-Antibiotic Combination Treatments: Antagonistic Impacts of Antibiotics on the Pharmacodynamics of Phage Therapy? · 2019

     No notice
247. 247.

     Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, et al Short Protocols in Molecular Biology: A Compendium of Methods from Current Protocols in Molecular Biology. John Wiley & Sons; 1995.

     Not in our library

248. 248.
     Complete Genome Sequence of Escherichia coli BW25113 · 2014

     No notice
249. 249.

     Ptashne M. A Genetic Switch: Phage Lambda Revisited. CSHL Press; 2004.

     Not in our library

250. 250.

     Ikeda H, Tomizawa J-I. Transducing fragments in generalized transduction by phage P1 I. Molecular origin of the fragments. Journal of Molecular Biology. 1966:226

     Not in our library10.1016/s0022-2836(66)80067-0

251. 251.

     Price MN, Ray J, Iavarone AT, Carlson HK, Ryan EM, Malmstrom RR, et al Oxidative Pathways of Deoxyribose and Deoxyribonate Catabolism. mSystems. 2019;4

     Not in our library10.1128/msystems.00297-18

252. 252.

     McCarthy DJ, Chen Y, Smyth GK. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res. 2012;40: 4288–4297.

     Not in our library10.1093/nar/gks042

253. 253.

     Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26: 139–140.

     Not in our library10.1093/bioinformatics/btp616

254. 254.

     Datta S, Costantino N, Court DL. A set of recombineering plasmids for gram-negative bacteria. Gene. 2006;379: 109–115.

     Not in our library10.1016/j.gene.2006.04.018

255. 255.
     KBase: The United States Department of Energy Systems Biology Knowledgebase · 2018

     No notice
256. 256.
     Trimmomatic: a flexible trimmer for Illumina sequence data · 2014

     No notice
257. 257.

     Kim D, Paggi JM, Park C, Bennett C, Salzberg SL. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019;37: 907–915.

     Not in our library10.1038/s41587-019-0201-4

258. 258.

     Pertea M, Pertea GM, Antonescu CM, Chang T-C, Mendell JT, Salzberg SL. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 2015;33: 290–295.

     Not in our library10.1038/nbt.3122

259. 259.
     Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 · 2014

     No notice
260. 260.

     Bak G, Lee J, Suk S, Kim D, Young Lee J, Kim K-S, et al Identification of novel sRNAs involved in biofilm formation, motility, and fimbriae formation in Escherichia coli. Sci Rep. 2015;5: 15287

     Not in our library10.1038/srep15287

Cited by papers we hold 3

• Broad-spectrum CRISPR-Cas13a enables efficient phage genome editing · 2022
  No notice
• Antiviral Resistance and Phage Counter Adaptation to Antibiotic-Resistant Extraintestinal Pathogenic <i>Escherichia coli</i> · 2021
  Not checked
• Systematic exploration of Escherichia coli phage–host interactions with the BASEL phage collection · 2021
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.