The role of iron in Mycobacterium smegmatis biofilm formation: the exochelin siderophore is essential in limiting iron conditions for biofilm formation but not for planktonic growth

Abstract

Summary Many species of mycobacteria form structured biofilm communities at liquid–air interfaces and on solid surfaces. Full development of Mycobacterium smegmatis biofilms requires addition of supplemental iron above 1 μM ferrous sulphate, although addition of iron is not needed for planktonic growth. Microarray analysis of the M. smegmatis transcriptome shows that iron‐responsive genes – especially those involved in siderophore synthesis and iron uptake – are strongly induced during biofilm formation reflecting a response to iron deprivation, even when 2 μM iron is present. The acquisition of iron under these conditions is specifically dependent on the exochelin synthesis and uptake pathways, and the strong defect of an iron–exochelin uptake mutant suggests a regulatory role of iron in the transition to biofilm growth. In contrast, although the expression of mycobactin and iron ABC transport operons is highly upregulated during biofilm formation, mutants in these systems form normal biofilms in low‐iron (2 μM) conditions. A close correlation between iron availability and matrix‐associated fatty acids implies a possible metabolic role in the late stages of biofilm maturation, in addition to the early regulatory role. M. smegmatis surface motility is similarly dependent on iron availability, requiring both supplemental iron and the exochelin pathway to acquire it.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 65

1. 1.

   Andrews SC, Robinson AK, Rodriguez-Quinones F. Bacterial iron homeostasis. FEMS Microbiol Rev. 2003;27:215-237.

   Not in our library10.1016/s0168-6445(03)00055-x

2. 2.

   Banin E, Vasil ML, Greenberg EP. Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci USA. 2005;102:11076-11081.

   Not in our library10.1073/pnas.0504266102

3. 3.

   Bardarov S, Bardarov S, Pavelka MS, Sambandamurthy V, Larsen M, Tufariello J, et al. Specialized transduction: an efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M. bovis BCG and M. smegmatis. Microbiology. 2002;148:3007-3017.

   Not in our library10.1099/00221287-148-10-3007

4. 4.

   Beenken KE, Dunman PM, McAleese F, Macapagal D, Murphy E, Projan SJ, et al. Global gene expression in Staphylococcus aureus biofilms. J Bacteriol. 2004;186:4665-4684.

   Not in our library10.1128/jb.186.14.4665-4684.2004

5. 5.

   Beloin C, Ghigo JM. Finding gene-expression patterns in bacterial biofilms. Trends Microbiol. 2005;13:16-19.

   Not in our library10.1016/j.tim.2004.11.008

6. 6.

   Beloin C, Valle J, Latour-Lambert P, Faure P, Kzreminski M, Balestrino D, et al. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol. 2004;51:659-674.

   Not in our library10.1046/j.1365-2958.2003.03865.x

7. 7.

   Berlutti F, Morea C, Battistoni A, Sarli S, Cipriani P, Superti F, et al. Iron availability influences aggregation, biofilm, adhesion and invasion of Pseudomonas aeruginosa and Burkholderia cenocepacia. Int J Immunopathol Pharmacol. 2005;18:661-670.

   Not in our library10.1177/039463200501800407

8. 8.

   Billman-Jacobe H, McConville MJ, Haites RE, Kovacevic S, Coppel RL. Identification of a peptide synthetase involved in the biosynthesis of glycopeptidolipids of Mycobacterium smegmatis. Mol Microbiol. 1999;33:1244-1253.

   Not in our library10.1046/j.1365-2958.1999.01572.x

9. 9.

   Carter G, Wu M, Drummond DC, Bermudez LE. Characterization of biofilm formation by clinical isolates of Mycobacterium avium. J Med Microbiol. 2003;52:747-752.

   Not in our library10.1099/jmm.0.05224-0

10. 10.

    Cho KH, Caparon MG. Patterns of virulence gene expression differ between biofilm and tissue communities of Streptococcus pyogenes. Mol Microbiol. 2005;57:1545-1556.

    Not in our library10.1111/j.1365-2958.2005.04786.x

11. 11.

    Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284:1318-1322.

    Not in our library10.1126/science.284.5418.1318

12. 12.

    Davey ME, O'Toole GA. Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev. 2000;64:847-867.

    Not in our library10.1128/mmbr.64.4.847-867.2000

13. 13.

    De Voss JJ, Rutter K, Schroeder BG, Barry CE. Iron acquisition and metabolism by mycobacteria. J Bacteriol. 1999;181:4443-4451.

    Not in our library10.1128/jb.181.15.4443-4451.1999

14. 14.
    The salicylate-derived mycobactin siderophores of Mycobacterium tuberculosis are essential for growth in macrophages · 2000

    Not checked
15. 15.

    Domka J, Lee J, Bansal T, Wood TK. Temporal gene-expression in Escherichia coli K-12 biofilms. Environ Microbiol. 2007;9:332-346.

    Not in our library10.1111/j.1462-2920.2006.01143.x

16. 16.

    Dussurget O, Rodriguez M, Smith I. An ideR mutant of Mycobacterium smegmatis has derepressed siderophore production and an altered oxidative-stress response. Mol Microbiol. 1996;22:535-544.

    Not in our library10.1046/j.1365-2958.1996.1461511.x

17. 17.

    Fiss EH, Yu S, Jacobs WR. Identification of genes involved in the sequestration of iron in mycobacteria: the ferric exochelin biosynthetic and uptake pathways. Mol Microbiol. 1994;14:557-569.

    Not in our library10.1111/j.1365-2958.1994.tb02189.x

18. 18.

    Frieden TR, Driver CR. Tuberculosis control: past 10 years and future progress. Tuberculosis (Edinb). 2003;83:82-85.

    Not in our library10.1016/s1472-9792(02)00060-4

19. 19.

    Gomez JE, McKinney JD. M. tuberculosis persistence, latency, and drug tolerance. Tuberculosis (Edinb). 2004;84:29-44.

    Not in our library10.1016/j.tube.2003.08.003

20. 20.

    Hall-Stoodley L, Lappin-Scott H. Biofilm formation by the rapidly growing mycobacterial species Mycobacterium fortuitum. FEMS Microbiol Lett. 1998;168:77-84.

    Not in our library10.1111/j.1574-6968.1998.tb13258.x

21. 21.

    Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol. 2004;2:95-108.

    Not in our library10.1038/nrmicro821

22. 22.

    Hall-Stoodley L, Brun OS, Polshyna G, Barker LP. Mycobacterium marinum biofilm formation reveals cording morphology. FEMS Microbiol Lett. 2006;257:43-49.

    Not in our library10.1111/j.1574-6968.2006.00143.x

23. 23.

    Honer Zu Bentrup K, Miczak A, Swenson DL, Russell DG. Characterization of activity and expression of isocitrate lyase in Mycobacterium avium and Mycobacterium tuberculosis. J Bacteriol. 1999;181:7161-7167.

    Not in our library10.1128/jb.181.23.7161-7167.1999

24. 24.

    Jeevarajah D, Patterson JH, McConville MJ, Billman-Jacobe H. Modification of glycopeptidolipids by an O-methyltransferase of Mycobacterium smegmatis. Microbiology. 2002;148:3079-3087.

    Not in our library10.1099/00221287-148-10-3079

25. 25.

    van Kessel JC, Hatfull GF. Recombineering in Mycobacterium tuberculosis. Nat Methods. 2007;4:147-152.

    Not in our library10.1038/nmeth996

26. 26.

    Krithika R, Marathe U, Saxena P, Ansari MZ, Mohanty D, Gokhale RS. A genetic locus required for iron acquisition in Mycobacterium tuberculosis. Proc Natl Acad Sci USA. 2006;103:2069-2074.

    Not in our library10.1073/pnas.0507924103

27. 27.

    LaMarca BB, Zhu W, Arceneaux JE, Byers BR, Lundrigan MD. Participation of fad and mbt genes in synthesis of mycobactin in Mycobacterium smegmatis. J Bacteriol. 2004;186:374-382.

    Not in our library10.1128/jb.186.2.374-382.2004

28. 28.

    Lazazzera BA. Lessons from DNA microarray analysis: the gene expression profile of biofilms. Curr Opin Microbiol. 2005;8:222-227.

    Not in our library10.1016/j.mib.2005.02.015

29. 29.

    McCune RM, Feldmann FM, Lambert HP, McDermott W. Microbial persistence. I. The capacity of tubercle bacilli to survive sterilization in mouse tissues. J Exp Med. 1966;123:445-468.

    Not in our library10.1084/jem.123.3.445

30. 30.

    Marsollier L, Aubry J, Coutanceau E, Andre JP, Small PL, Milon G, et al. Colonization of the salivary glands of Naucoris cimicoides by Mycobacterium ulcerans requires host plasmatocytes and a macrolide toxin, mycolactone. Cell Microbiol. 2005;7:935-943.

    Not in our library10.1111/j.1462-5822.2005.00521.x

31. 31.

    Martinez A, Torello S, Kolter R. Sliding motility in mycobacteria. J Bacteriol. 1999;181:7331-7338.

    Not in our library10.1128/jb.181.23.7331-7338.1999

32. 32.

    Milano A, Forti F, Sala C, Riccardi G, Ghisotti D. Transcriptional regulation of furA and katG upon oxidative stress in Mycobacterium smegmatis. J Bacteriol. 2001;183:6801-6806.

    Not in our library10.1128/jb.183.23.6801-6806.2001

33. 33.

    Moorthy S, Watnick PI. Identification of novel stage-specific genetic requirements through whole genome transcription profiling of Vibrio cholerae biofilm development. Mol Microbiol. 2005;57:1623-1635.

    Not in our library10.1111/j.1365-2958.2005.04797.x

34. 34.

    O'Toole G, Kaplan HB, Kolter R. Biofilm formation as microbial development. Annu Rev Microbiol. 2000;54:49-79.

    Not in our library10.1146/annurev.micro.54.1.49

35. 35.

    Ojha A, Anand M, Bhatt A, Kremer L, Jacobs WR, Hatfull GF. GroEL1: a dedicated chaperone involved in mycolic acid biosynthesis during biofilm formation in mycobacteria. Cell. 2005;123:861-873.

    Not in our library10.1016/j.cell.2005.09.012

36. 36.

    Ojha AK, Varma S, Chatterji D. Synthesis of an unusual polar glycopeptidolipid in glucose-limited culture of Mycobacterium smegmatis. Microbiology. 2002;148:3039-3048.

    Not in our library10.1099/00221287-148-10-3039

37. 37.

    Panina EM, Mironov AA, Gelfand MS. Comparative genomics of bacterial zinc regulons: enhanced ion transport, pathogenesis, and rearrangement of ribosomal proteins. Proc Natl Acad Sci USA. 2003;100:9912-9917.

    Not in our library10.1073/pnas.1733691100

38. 38.

    Patterson JH, McConville MJ, Haites RE, Coppel RL, Billman-Jacobe H. Identification of a methyltransferase from Mycobacterium smegmatis involved in glycopeptidolipid synthesis. J Biol Chem. 2000;275:24900-24906.

    Not in our library10.1074/jbc.m000147200

39. 39.

    Pruss BM, Besemann C, Denton A, Wolfe AJ. A complex transcription network controls the early stages of biofilm development by Escherichia coli. J Bacteriol. 2006;188:3731-3739.

    Not in our library10.1128/jb.01780-05

40. 40.

    Pysz MA, Conners SB, Montero CI, Shockley KR, Johnson MR, Ward DE, Kelly RM. Transcriptional analysis of biofilm formation processes in the anaerobic, hyperthermophilic bacterium Thermotoga maritima. Appl Environ Microbiol. 2004;70:6098-6112.

    Not in our library10.1128/aem.70.10.6098-6112.2004

Cited by papers we hold 3

• In Vitro Cultivation of 'Unculturable' Oral Bacteria, Facilitated by Community Culture and Media Supplementation with Siderophores. · 2016
  Not checked
• Thiol reductive stress induces cellulose-anchored biofilm formation in Mycobacterium tuberculosis · 2016
  No notice
• Growth of Mycobacterium tuberculosis biofilms containing free mycolic acids and harbouring drug‐tolerant bacteria · 2008
  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.