Skip to main content
PMC home page
Science Progress logoLink to Science Progress
. 2010 Mar 1;93(1):7–36. doi: 10.3184/003685009X12605525292307

Life in the Gut: Microbial responses to Stress in the Gastrointestinal Tract

Petra Louis 1, Conor P O'Byrne 2,✉
PMCID: PMC10365543  PMID: 20222354

Abstract

The complex physical and chemical conditions encountered in the gut present a range of physiological challenges to both the commensal microbiota and to pathogenic microorganisms attempting to colonise the gut. The innate immune system of the host, the host's diet and the microbial population present in the gut all contribute to the chemical complexity of the environment. The huge population of microorganisms in the gut also has a significant impact on the physicochemical properties of the gut environment. By focussing on some of the key physical and chemical stresses encountered by microorganisms in the gut, some of the molecular responses are described. Some promising new experimental approaches are outlined for studying the behaviour of microorganisms and their communities within the gut environment.

Keywords: commensal microbiota, pathogenic microorganisms, gut, anti-microbial compounds, short chain fatty acids, bacteriocins

Full Text

The Full Text of this article is available as a PDF (636.3 KB).

References

  • 1.Mukherjee S., Vaishnava S., and Hooper L.V. (2008) Multi-layered regulation of intestinal antimicrobial defense. Cell. Mol. Life Sci., 65(19), 3019–3027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Nuding S., Zabel L.T., Enders C., Porter E., Fellermann K., Wehkamp J., Mueller H.A.G., and Stange E.F. (2009) Antibacterial activity of human defensins on anaerobic intestinal bacterial species: a major role of HBD-3. Microb. Infect., 11(3), 384–393. [DOI] [PubMed] [Google Scholar]
  • 3.Meyer-Hoffert U., Hornef M.W., Henriques-Normark B., Axelsson L.G., Midtvedt T., Pütsep K., and Andersson M. (2008) Secreted enteric antimicrobial activity localises to the mucus surface layer. Gut, 57(6), 764–771. [DOI] [PubMed] [Google Scholar]
  • 4.Mestecky J., and Russell M.W. (2009) Specific antibody activity, glycan heterogeneity and polyreactivity contribute to the protective activity of S-IgA at mucosal surfaces. Immunol. Lett., 124(2), 57–62. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Raffatellu M., George M.D., Akiyama Y., Hornsby M.J., Nuccio S.P., Paixao T.A., Butler B.P., Chu H., Santos R.L., Berger T., Mak T.W., Tsolis R.M., Bevins C.L., Solnick J.V., Dandekar S., and Bäumler A.J. (2009) Lipocalin-2 resistance confers an advantage to Salmonella enterica Serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe, 5(5), 476–486. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Gillor O., Etzion A., and Riley M.A. (2008) The dual role of bacteriocins as anti- and probiotics. Appl. Microbiol. Biotechnol., 81(4), 591–606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Nes I.F., Yoon S.S., and Diep D.B. (2007) Ribosomally synthesiszed anti-microbial peptides (bacteriocins) in lactic acid bacteria: A review. Food Sci. Biotechnol., 16(5), 675–690. [Google Scholar]
  • 8.Kraus D., and Peschel A. (2006) Molecular mechanisms of bacterial resistance to antimicrobial peptides. Curr. Top. Microbiol. Immunol., 306, 231–250. [DOI] [PubMed] [Google Scholar]
  • 9.Manach C., Scalbert A., Morand C., Rémésy C., and Jiménez L. (2004) Polyphenols: Food sources and bioavailability. Am. J. Clin. Nutr., 79(5), 727–747. [DOI] [PubMed] [Google Scholar]
  • 10.Aura A.M. (2008) Microbial metabolism of dietary phenolic compounds in the colon. Phytochem. Rev., 7(3), 407–429. [Google Scholar]
  • 11.Selma M.V., Espin J.C., and Tomas-Barberan F.A. (2009) Interaction between Phenolics and Gut Microbiota: Role in Human Health. J. Agric. Food Chem., 57(15), 6485–6501. [DOI] [PubMed] [Google Scholar]
  • 12.Puupponen-Pimiä R., Nohynek L., Alakomi H.L., and Oksman-Caldentey K.M. (2005) The action of berry phenolics against human intestinal pathogens. Biofactors, 23(4), 243–251. [DOI] [PubMed] [Google Scholar]
  • 13.Chesson A., Stewart C.S., and Wallace R.J. (1982) Influence of plant phenolic acids on growth and cellulolytic activity of rumen bacteria. Appl. Environ. Microbiol., 44(3), 597–603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Licandro-Seraut H., Gury J., Tran N.P., Barthelmebs L., and Cavin J.F. (2008) Kinetics and intensity of the expression of genes involved in the stress response tightly induced by phenolic acids in Lactobacillus plantarum. J. Mol. Microbiol. Biotechnol., 14(1-3), 41–47. [DOI] [PubMed] [Google Scholar]
  • 15.Begley M., Gahan C.G.M., and Hill C. (2005) The interaction between bacteria and bile. FEMS Microbiol. Rev., 29(4), 625–651. [DOI] [PubMed] [Google Scholar]
  • 16.Northfield T.C., and McColl I. (1973) Postprandial concentrations of free and conjugated bile acids down the length of the normal human small intestine. Gut, 14(7), 513–518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Hofmann A.F., and Eckmann L. (2006) How bile acids confer gut mucosal protection against bacteria. Proc. Natl. Acad. Sci. USA, 103(12), 4333–4334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Sung J.Y., Shaffer E.A., and Costerton J.W. (1993) Antibacterial activity of bile salts against common biliary pathogens. Effects of hydrophobicity of the molecule and in the presence of phospholipids. Dig. Dis. Sci., 38(11), 2104–2112. [DOI] [PubMed] [Google Scholar]
  • 19.Inagaki T., Moschetta A., Lee Y.K., Peng L., Zhao G., Downes M., Yu R.T., Shelton J.M., Richardson J.A., Repa J.J., Mangelsdorf D.J., and Kliewer S.A. (2006) Regulation of antibacterial defense in the small intestine by the nuclear bile acid receptor. Proc. Natl. Acad. Sci. USA, 103(10), 3920–3925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Lacroix F.J.C., Avoyne C., Pinault C., Popoff M.Y., and Pardon P. (1995) Salmonella typhimurium TnphoA mutants with increased sensitivity to biological and chemical detergents. Res. Microbiol., 146(8), 659–670. [DOI] [PubMed] [Google Scholar]
  • 21.Thanassi D.G., Cheng L.W., and Nikaido H. (1997) Active efflux of bile salts by Escherichia coli. J. Bacteriol., 179(8), 2512–2518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Nesper J., Lauriano C.M., Klose K.E., Kapfhammer D., Kraiß A., and Reidl J. (2001) Characterization of Vibrio cholerae Ol El Tor galU and galE mutants: Influence on lipopolysaccharide structure, colonization, and biofilm formation. Infect. Immun., 69(1), 435–445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Lin J., Overbye Michel L., and Zhang Q. (2002) CmeABC functions as a multidrug efflux system in Campylobacter jejuni. Antimicrob. Agents Chemother., 46(7), 2124–2131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Heithoff D.M., Enioutina E.Y., Daynes R.A., Sinsheimer R.L., Low D.A., and Mahan M.J. (2001) Salmonella DNA adenine methylase mutants confer cross-protective immunity. Infect. Immun., 69(11), 6725–6730. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Le Breton Y., Mazé A., Hartke A., Lemarinier S., Auffray Y., and Rincé A. (2002) Isolation and characterization of bile salts-sensitive mutants of Enter-ococcus faecalis. Curr. Microbiol., 45(6), 434–439. [DOI] [PubMed] [Google Scholar]
  • 26.Leverrier P., Dimova D., Pichereau V., Auffray Y., Boyaval P., and Jan G. (2003) Susceptibility and adaptive response to bile salts in Propionibacterium freudenreichii: Physiological and proteomic anlysis. Appl. Environ. Microbiol., 69(7), 3809–3818. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Bernstein C., Bernstein H., Payne C.M., Beard S.E., and Schneider J. (1999) Bile salt activation of stress response promoters in Escherichia coli. Curr. Microbiol., 39(2), 68–72. [DOI] [PubMed] [Google Scholar]
  • 28.Jones B.V., Begley M., Hill C., Gahan C.G.M., and Marchesi J.R. (2008) Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. Proc. Natl. Acad. Sci. USA, 105(36), 13580–13585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Dussurget O., Cabanes D., Dehoux P., Lecuit M., Buchrieser C., Glaser P., and Cossart P. (2002) Listeria monocytogenes bile salt hydrolase is a PrfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis. Mol. Microbiol., 45(4), 1095–1106. [DOI] [PubMed] [Google Scholar]
  • 30.Grill J.P., Cayuela C., Antoine J.M., and Schneider F. (2000) Isolation and characterization of a Lactobacillus amylovorus mutant depleted in conjugated bile salt hydrolase activity: Relation between activity and bile salt resistance. J. Appl. Microbiol., 89(4), 553–563. [DOI] [PubMed] [Google Scholar]
  • 31.Chowdhury R., Sahu G.K., and Das J. (1996) Stress response in pathogenic bacteria. J. Biosci., 21(2), 149–160. [Google Scholar]
  • 32.Sleator R.D., Clifford T., and Hill C. (2007) Gut osmolarity: A key environmental cue initiating the gastrointestinal phase of Listeria monocytogenes infection? Med. Hypotheses, 69(5), 1090–1092. [DOI] [PubMed] [Google Scholar]
  • 33.Wrong O., and Metcalfegibson A. (1965) The electrolyte content faeces. Proc. R. Soc. Med., 58(12), 1007–1009. [PMC free article] [PubMed] [Google Scholar]
  • 34.Gowrishankar J., and Manna D. (1996) How is osmotic regulation of transcription of the Escherichia coli proU operon achieved? A review and a model. Genetica, 97(3), 363–378. [DOI] [PubMed] [Google Scholar]
  • 35.Culham D.E., Dalgado C., Gyles C.L., Mamelak D., MacLellan S., and Wood J.M. (1998) Osmoregulatory transporter ProP influences colonization of the urinary tract by Escherichia coli. Microbiology, 144(1), 91–102. [DOI] [PubMed] [Google Scholar]
  • 36.Fraser K.R., Harvie D., Coote P.J., and O'Byrne C.P. (2000) Identification and characterization of an ATP binding cassette L-carnitine transporter in Listeria monocytogenes. Appl. Environ. Microbiol., 66(11), 4696–4704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Sleator R.D., Wouters J., Gahan C.G.M., Abee T., and Hill C. (2001) Analysis of the Role of OpuC, an Osmolyte Transport System, in Salt Tolerance and Virulence Potential of Listeria monocytogenes. Appl. Environ. Microbiol., 67(6), 2692–2698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Foster J.W. (2004) Escherichia coli acid resistance: Tales of an amateur acidophile. Nat. Rev. Microbiol., 2(11), 898–907. [DOI] [PubMed] [Google Scholar]
  • 39.Ho J.L., Shands K.N., Friedland G., Eckind P., and Fraser D.W. (1986) An outbreak of type 4b Listeria monocytogenes infection involving patients from eight Boston hospitals. Arch. Intern. Med., 146(3), 520–524. [PubMed] [Google Scholar]
  • 40.Lin J., Smith M.P., Chapin K.C., Baik H.S., Bennett G.N., and Foster J.W. (1996) Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Appl. Environ. Microbiol., 62(9), 3094–3100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Walker A.W., Duncan S.H., McWilliam Leitch E.C., Child M.W., and Flint H.J. (2005) pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl. Environ. Microbiol., 71(7), 3692–3700. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Duncan S.H., Louis P., Thomson J.M., and Flint H.J. (2009) The role of pH in determining the species composition of the human colonic microbiota. Environ. Microbiol., 11(8), 2112–2122. [DOI] [PubMed] [Google Scholar]
  • 43.Weeks D.L., Eskandari S., Scott D.R., and Sachs G. (2000) A H+-gated urea channel: The link between Helicobacter pylori urease and gastric colonization. Science, 287(5452), 482–485. [DOI] [PubMed] [Google Scholar]
  • 44.Skouloubris S., Thiberge J.M., Labigne A., and De Reuse H. (1998) The Helicobacter pylori UreI protein is not involved in urease activity but is essential for bacterial survival in vivo. Infect. Immun., 66(9), 4517–4521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.Cotter P.D., and Hill C. (2003) Surviving the acid test: Responses of gram-positive bacteria to low pH. Microbiol. Mol. Biol. Rev., 67(3), 429–453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Ryan S., Begley M., Gahan C.G.M., and Hill C. (2009) Molecular characterization of the arginine deiminase system in Listeria monocytogenes: Regulation and role in acid tolerance. Environ. Microbiol., 11(2), 432–445. [DOI] [PubMed] [Google Scholar]
  • 47.Torres A.G. (2009) The cad locus of Enterobacteriaceae: More than just lysine decarboxylation. Anaerobe, 15(1-2), 1–6. [DOI] [PubMed] [Google Scholar]
  • 48.Duncan C., Dougall H., Johnston P., Green S., Brogan R., Leifert C., Smith L., Golden M., and Benjamin N. (1995) Chemical generation of nitric oxide in the mouth from the enterosalivary circulation of dietary nitrate. Nat. Med., 1(6), 546–551. [DOI] [PubMed] [Google Scholar]
  • 49.Benjamin N., O'Driscoll F., Dougall H., Duncan C., Smith L., Golden M., and McKenzie H. (1994) Stomach NO synthesis. Nature, 368(6471), 502. [DOI] [PubMed] [Google Scholar]
  • 50.Dykhuizen R.S., Frazer R., Duncan C., Smith C.C., Golden M., Benjamin N., and Leifert C. (1996) Antimicrobial effect of acidified nitrite on gut pathogens: Importance of dietary nitrate in host defense. Antimicrob. Agents Chemother., 40(6), 1422–1425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Bourret T.J., Porwollik S., McClelland M., Zhao R., Greco T., Ischiropoulos H., and Vázquez-Torres A. (2008) Nitric oxide antagonizes the acid tolerance response that protects Salmonella against innate gastric defenses. PLoS ONE, 3(3). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Two-Component Signal Transduction (1995) ASM Press, Washington, D.C. [Google Scholar]
  • 53.Podar M. (2007) Two-Component Systems in Microbial Communities: Approaches and Resources for Generating and Analyzing Metagenomic Data Sets. Methods Enzymol., 422, 32–46. [DOI] [PubMed] [Google Scholar]
  • 54.Schell M.A., Karmirantzou M., Snel B., Vilanova D., Berger B., Pessi G., Zwahlen M.C., Desiere F., Bork P., Delley M., Pridmore R.D., and Arigoni F. (2002) The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc. Natl. Acad. Sci. USA, 99(22), 14422–14427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.Kuwahara T., Yamashita A., Hirakawa H., Nakayama H., Toh H., Okada N., Kuhara S., Hattori M., Hayashi T., and Ohnishi Y. (2004) Genomic analysis of Bacteroides fragilis reveals extensive DNA inversions regulating cell surface adaptation. Proc. Natl. Acad. Sci. USA, 101(41), 14919–14924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56.Calva E., and Oropeza R. (2006) Two-component signal transduction systems, environmental signals, and virulence. Microb. Ecol., 51(2), 166–176. [DOI] [PubMed] [Google Scholar]
  • 57.Dorman C.J., Chatfield S., Higgins C.F., Hayward C., and Dougan G. (1989) Characterization of porin and ompR mutants of a virulent strain of Salmonella typhimurium: ompR mutants are attenuated in vivo. Infect. Immun., 57(7), 2136–2140. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Fass E., and Groisman E.A. (2009) Control of Salmonella pathogenicity island-2 gene expression. Curr. Opin. Microbiol., 12(2), 199–204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.Miller S.I., Kukral A.M., and Mekalanos J.J. (1989) A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc. Natl. Acad. Sci. USA, 86(13), 5054–5058. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Hohmann E.L., Oletta C.A., Killeen K.P., and Miller S.I. (1996) phoPyphoQ-deleted Salmonella typhi (Ty800) is a safe and immunogenic single-dose typhoid fever vaccine in volunteers. J. Infect. Dis., 173(6), 1408–1414. [DOI] [PubMed] [Google Scholar]
  • 61.Merighi M., Ellermeier C.D., Slauch J.M., and Gunn J.S. (2005) Resolvase-in vivo expression technology analysis of the Salmonella enterica serovar typhimurium PhoP and PmrA regulons in BALByc mice. J. Bacteriol., 187(21), 7407–7416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Gunn J.S. (2008) The Salmonella PmrAB regulon: lipopolysaccharide modifications, antimicrobial peptide resistance and more. Trends Microbiol., 16(6), 284–290. [DOI] [PubMed] [Google Scholar]
  • 63.Gunn J.S., Ryan S.S., Van Velkinburgh J.C., Ernst R.K., and Miller S.I. (2000) Genetic and functional analysis of a PmrA-PmrB-regulated locus necessary for lipopolysaccharide modification, antimicrobial peptide resistance, and oral virulence of Salmonella enterica serovar typhimurium. Infect. Immun., 68(11), 6139–6146. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Kazmierczak M.J., Wiedmann M., and Boor K.J. (2005) Alternative sigma factors and their roles in bacterial virulence. Microbiol. Mol. Biol. Rev., 69(4), 527–543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65.O'Byrne C.P., and Karatzas K.A.G. (2008) The Role of Sigma B (σB) in the Stress Adaptations of Listeria monocytogenes: Overlaps Between Stress Adaptation and Virulence. Adv. Appl. Microbiol., 65, 115–140. [DOI] [PubMed] [Google Scholar]
  • 66.Toledo-Arana A., Dussurget O., Nikitas G., Sesto N., Guet-Revillet H., Balestrino D., Loh E., Gripenland J., Tiensuu T., Vaitkevicius K., Barthelemy M., Vergassola M., Nahori M.A., Soubigou G., Régnault B., Coppée J.Y., Lecuit M., Johansson J., and Cossart P. (2009) The Listeria transcriptional landscape from saprophytism to virulence. Nature, 459(7249), 950–956. [DOI] [PubMed] [Google Scholar]
  • 67.Chaturongakul S., Raengpradub S., Wiedmann M., and Boor K.J. (2008) Modulation of stress and virulence in Listeria monocytogenes. Trends Microbiol., 16(8), 388–396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 68.Kim H., Marquis H., and Boor K.J. (2005) σB contributes to Listeria monocytogenes invasion by controlling expression of inlA and inlB. Microbiology, 151(10), 3215–3222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 69.Garner M.R., Njaa B.L., Wiedmann M., and Boor K.J. (2006) Sigma B contributes to Listeria monocytogenes gastrointestinal infection but not to systemic spread in the guinea pig infection model. Infect. Immun., 74(2), 876–886. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 70.Hecker M., Pané-Farré J., and Völker U. (2007) SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu. Rev. Microbiol., 61, 215–236. [DOI] [PubMed] [Google Scholar]
  • 71.Audia J.P., Webb C.C., and Foster J.W. (2001) Breaking through the acid barrier: An orchestrated response to proton stress by enteric bacteria. Int. J. Med. Microbiol., 291(2), 97–106. [DOI] [PubMed] [Google Scholar]
  • 72.Small P., Blankenhorn D., Welty D., Zinser E., and Slonczewski J.L. (1994) Acid and base resistance in Escherichia coli and Shigella flexneri: Role of rpoS and growth pH. J. Bacteriol., 176(6), 1729–1737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 73.Hengge-Aronis R. (2000) The general stress response in Escherichia coli. Bacterial stress responses, Storz G., and Hengge-Aronis R. (eds.), pp. 161–178. ASM Press, Washington, D.C. [Google Scholar]
  • 74.Nielsen A.T., Dolganov N.A., Otto G., Miller M.C., Wu C.Y., and Schoolnik G.K. (2006) RpoS controls the Vibrio cholerae mucosal escape response. PLoS Pathog., 2(10). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 75.Klauck E., Typas A., and Hengge R. (2007) The sigmaS subunit of RNA polymerase as a signal integrator and network master regulator in the general stress response in Escherichia coli. Sci. Prog., 90(Pt 2–3), 103–127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 76.Bougdour A., Cunning C., Baptiste P.J., Elliott T., and Gottesman S. (2008) Multiple pathways for regulation of σS (RpoS) stability in Escherichia coli via the action of multiple anti-adaptors. Mol. Microbiol., 68(2), 298–313. [DOI] [PubMed] [Google Scholar]
  • 77.Rowley G., Spector M., Kormanec J., and Roberts M. (2006) Pushing the envelope: Extracytoplasmic stress responses in bacterial pathogens. Nat. Rev. Microbiol., 4(5), 383–394. [DOI] [PubMed] [Google Scholar]
  • 78.Crouch M.L., Becker L.A., Bang I.S., Tanabe H., Ouellette A.J., and Fang F.C. (2005) The alternative sigma factor σE is required for resistance of Salmonella enterica serovar Typhimurium to anti-microbial peptides. Mol. Microbiol., 56(3), 789–799. [DOI] [PubMed] [Google Scholar]
  • 79.Kovacikova G., and Skorupski K. (2002) The alternative sigma factor σE plays an important role in intestinal survival and virulence in Vibrio cholerae. Infect. Immun., 70(10), 5355–5362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 80.Ades S.E. (2004) Control of the alternative sigma factor σE in Escherichia coli. Curr. Opin. Microbiol., 7(2), 157–162. [DOI] [PubMed] [Google Scholar]
  • 81.King T., Seeto S., and Ferenci T. (2006) Genotype-by-environment interactions influencing the emergence of rpoS mutations in Escherichia coli populations. Genetics, 172(4), 2071–2079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 82.Abram F., Starr E., Karatzas K.A.G., Matlawska-Wasowska K., Boyd A., Wiedmann M., Boor K.J., Connally D., and O'Byrne C.P. (2008) Identification of components of the sigma B regulon in Listeria monocytogenes that contribute to acid and salt tolerance. Appl. Environ. Microbiol., 74(22), 6848–6858. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 83.Nyström T. (2004) Growth versus maintenance: A trade-off dictated by RNA polymerase availability and sigma factor competition? Mol. Microbiol., 54(4), 855–862. [DOI] [PubMed] [Google Scholar]
  • 84.Holman H.Y., Wozei E., Lin Z., Comolli L.R., Ball D.A., Borglin S., Fields M.W., Hazen T.C., and Downing K.H. (2009) Real-time molecular monitoring of chemical environment in obligate anaerobes during oxygen adaptive response. Proc. Natl. Acad. Sci. USA, 106(31), 12599–12604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 85.Garcia D.E., Baidoo E.E., Benke P.I., Pingitore F., Tang Y.J., Villa S., and Keasling J.D. (2008) Separation and mass spectrometry in microbial metabolomics. Curr. Opin. Microbiol., 11(3), 233–239. [DOI] [PubMed] [Google Scholar]
  • 86.Mahan M.J., Heithoff D.M., Sinsheimer R.L., and Low D.A. (2000) Assessment of bacterial pathogenesis by analysis of gene expression in the host. Annu. Rev. Genet., 34, 139–164. [DOI] [PubMed] [Google Scholar]
  • 87.Rediers H., Rainey P.B., Vanderleyden J., and De Mot R. (2005) Unraveling the secret lives of bacteria: Use of in vivo expression technology and differential fluorescence induction promoter traps as tools for exploring niche-specific gene expression. Microbiol. Mol. Biol. Rev., 69(2), 217–261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 88.Bron P.A., Meijer M., Bongers R.S., De Vos W.M., and Kleerebezem M. (2007) 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., 103(5), 1424–1434. [DOI] [PubMed] [Google Scholar]
  • 89.Lombardo M.J., Michalski J., Martinez-Wilson H., Morin C., Hilton T., Osorio C.G., Nataro J.P., Tacket C.O., Camilli A., and Kaper J.B. (2007) An in vivo expression technology screen for Vibrio cholerae genes expressed in human volunteers. Proc. Natl. Acad. Sci. USA, 104(46), 18229–18234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 90.Hardy J., Francis K.P., DeBoer M., Chu P., Gibbs K., and Contag C.H. (2004) Extracellular Replication of Listeria monocytogenes in the Murine Gall Bladder. Science, 303(5659), 851–853. [DOI] [PubMed] [Google Scholar]
  • 91.Cronin M., Sleator R.D., Hill C., Fitzgerald G.F., and Van Sinderen D. (2008) Development of a luciferase-based reporter system to monitor Bifidobacterium breve UCC2003 persistence in mice. BMC Microbiol., 8, 161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 92.Denou E., Berger B., Barretto C., Panoff J.M., Arigoni F., and Brüssow H. (2007) Gene expression of commensal Lactobacillus johnsonii strain NCC533 during in vitro growth and in the murine gut. J. Bacteriol., 189(22), 8109–8119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 93.Yuan J., Wang B., Sun Z., Bo X., Yuan X., He X., Zhao H., Du X., Wang F., Jiang Z., Zhang L., Jia L., Wang Y., Wei K., Wang J., Zhang X., Sun Y., Huang L., and Zeng M. (2008) Analysis of host-inducing proteome changes in Bifidobacterium longum NCC2705 grown in vivo. J. Proteome Res., 7(1), 375–385. [DOI] [PubMed] [Google Scholar]
  • 94.Gevaert K., Van Damme P., Ghesquière B., Impens F., Martens L., Helsens K., and Vandekerckhove J. (2007) A la carte proteomics with an emphasis on gel-free techniques. Proteomics, 7(16), 2698–2718. [DOI] [PubMed] [Google Scholar]
  • 95.Pichon C., and Felden B. (2008) Small RNA gene identification and mRNA target predictions in bacteria. Bioinformatics, 24(24), 2807–2813. [DOI] [PubMed] [Google Scholar]
  • 96.Flint H.J., Duncan S.H., and Louis P. (2009) Gut microbial ecology. Designing functional foods: measuring and controlling food structure breakdown and nutrient absorption, McClements D.J., and Decker E.A. (eds.), pp. 38–67. Woodhead Publishing Limited, Cambridge. [Google Scholar]
  • 97.Kurokawa K., Itoh T., Kuwahara T., Oshima K., Toh H., Toyoda A., Takami H., Morita H., Sharma V.K., Srivastava T.P., Taylor T.D., Noguchi H., Mori H., Ogura Y., Ehrlich D.S., Itoh K., Takagi T., Sakaki Y., Hayashi T., and Hattori M. (2007) Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res., 14(4), 169–181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 98.Vieites J.M., Guazzaroni M.E., Beloqui A., Golyshin P.N., and Ferrer M. (2009) Metagenomics approaches in systems microbiology. FEMS Microbiol. Rev., 33(1), 236–255. [DOI] [PubMed] [Google Scholar]
  • 99.Verberkmoes N.C., Russell A.L., Shah M., Godzik A., Rosenquist M., Halfvarson J., Lefsrud M.G., Apajalahti J., Tysk C., Hettich R.L., and Jansson J.K. (2009) Shotgun metaproteomics of the human distal gut microbiota. ISME J., 3(2), 179–189. [DOI] [PubMed] [Google Scholar]

Articles from Science Progress are provided here courtesy of SAGE Publications

RESOURCES