Bacterial stress response as an adaptation to life in a soil environment

Polish Journal of Environmental Studies

Volumn 22, Issue 6, 2013, Pages 1577-1587

  Świeciło, Agata ^a   Zych Wezyk, Iwona ^a  

^a UNIVERSITY OF LIFE SCIENCES IN LUBLIN   (Poland)

Author keywords

General stress response; Nutrient starvation; Soil micro organisms; Stringent response

Indexed keywords

EID: 84890368665     PISSN: 12301485     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (103)

1. SCHIMEL J., BALSER T., WALLENSTEIN M. Microbial stress-response physiology and its implications for ecosystem function. Ecology 88, (6), 1386, 2007.
2. KOLTER R., SIEGELE D.A., TORMO A. The stationary phase of the bacterial life cycle. Annu. Rev. Microbiol. 47, 855, 1993.
3. GRAY J.V., PETSKO G.A., JOHNSTON G.C., RINGE D., SINGER R.A., WERNER-WASHBURNE M. "Sleeping beauty": quiescence in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 68, (2), 187, 2004.
4. HELMANN J.D., WU M.F.W., KOBEL P.A., GAMO F-J., WILSON M., MORSHEDI M.M., NAVRE M., PADDON C. Global Transcriptional Response of Bacillus subtilis to Heat Shock. J. Bacteriol. 183, (24), 7318, 2001.
5. ZHAO K., LIU M., BURGESS R.R. The global transcriptional response of Escherichia coli to induced σ32 protein involves σ32 regulon activation followed by inactivation and degradation of σ32 in vivo. J. Biol. Chem. 280, (18), 17758, 2005.
6. BECKMANN R.P., MIZZEN L., WELCH W. Interaction of Hsp70 with newly synthesized proteins: implications for protein folding and assembly. Science 248, 850, 1990.
7. REEVE C.A., AMY P.S., MATIN A. Role of protein synthesis in the survival of carbon-starved Escherichia coli K-12. J. Bacteriol. 160, (3), 1041, 1984.
8. LANGE R., HENGGE-ARONIS R. Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol. Microbiol. 5, (1), 49, 1991.
9. HENGGE-ARONIS R. Back to log phase: sigma S as a global regulator in the osmotic control of gene expression in Escherichia coli. Mol. Microbiol. 21, (5), 887, 1996.
10. HECKER M., PANÉ-FARRÉ J., VÖLKER U. SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu. Rev. Microbiol. 61, 215, 2007.
11. CASES I., USSERY D.W., DE LORENZO V. The sigma54 regulon (sigmulon) of Pseudomonas putida. Environ Microbiol. 5, (12), 1281, 2003.
12. CASHEL M., GENTRY D.M., HERNANDEZ V.J., VINELLA D. The stringent response. In Escherichia coli and Salmonella typhimurium Cellular and Molecular Biology. (F. C. Neidhardt, Ed. in Chief). ASM Press, Washington D.C. 1, 1458, 1996.
13. GENTRY D.R., CASHEL M. Mutational analysis of the Escherichia coli spoT gene identifies distinct but overlapping regions involved in ppGpp synthesis and degradation. Mol. Microbiol. 19, (6), 1373, 1996.
14. MITTENHUBER G. Comparative genomics and evolution of genes encoding bacterial (p)ppGpp synthetases/ hydrolases (the Rel, RelA and SpoT proteins). J. Mol. Microbiol. Biotechnol. 3, (4), 585, 2001.
15. ARTSIMOVITCH I., PATLAN V., SEKINE S., VASSYLYEVA M.N., HOSAKA T., OCHI K., YOKOYAMA S., VASSYLYEV D.G. Structural basis for transcription regulation by alarmone ppGpp. Cell 117, (3), 299, 2004.
16. JISHAGE M., KVINT K., SHINGLER V., NYSTRÖM T. Regulation of sigma factor competition by the alarmone ppGpp. Genes Dev. 16, (10), 1260, 2002.
17. MAGNUSSON L.U., FAREWELL A., NYSTRÖM T. ppGpp: a global regulator in Escherichia coli. Trends Microbiol. 13, (5), 236, 2005.
18. NYSTRÖM T. Stationary-phase physiology. Annu. Rev. Microbiol. 58, 161, 2004.
19. HUISMAN G.W., SIEGELE M., ZAMBRANO M., KOLTER R. Morphological and Physiological Changes during Stationary Phase. American Society for Microbiology Press, Washington, DC 1996.
20. ALMIRÓN M., LINK A.J., FURLONG D., KOLTER R. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 6, (12B), 2646, 1992.
21. NAIR S., FINKEL S.E. Dps protects cells against multiple stresses during stationary phase. J. Bacteriol. 186, (13), 4192, 2004.
22. MARTINEZ A., KOLTER R. Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J. Bacteriol. 179, (16), 5188, 1997.
23. BARKER M.M., GAAL T., JOSAITIS C.A., GOURSE R.L. Mechanism of regulation of transcription initiation by ppGpp. I. Effects of ppGpp on transcription initiation in vivo and in vitro. J. Mol. Biol. 305, (4), 673, 2001.
24. GROAT R.G., SCHULTZ J.E., ZYCHLINSKY E., BOCKMAN A., MATIN A. Starvation proteins in Escherichia coli: kinetics of synthesis and role in starvation survival. J. Bacteriol. 168, (2), 486, 1986.
25. WEICHART D., QUERFURTH N., DREGER M., HENGGE-ARONIS R. Global role for ClpP-containing proteases in stationary-phase adaptation of Escherichia coli. J. Bacteriol. 185, (1), 115, 2003.
26. FAREWELL A., DIEZ A.A., DIRUSSO C.C., NYSTRÖM T. Role of the Escherichia coli FadR regulator in stasis survival and growth phase-dependent expression of the uspA, fad, and fab genes. J. Bacteriol. 178, (22), 6443, 1996.
27. GROSSMAN A.D., TAYLOR W.E., BURTON Z.F., BURGESS R.R., GROSS C.A. Stringent response in Escherichia coli induces expression of heat shock proteins. J. Mol. Biol. 186, (2), 357, 1985.
28. GIVSKOV M., EBERL L., MØLLER S., POULSEN L.K., MOLIN S. Responses to nutrient starvation in Pseudomonas putida KT2442: analysis of general cross-protection, cell shape, and macromolecular content. J. Bacteriol. 176, (1), 7, 1994.
29. RIVAS M., SEEGER M., HOLMES D.S., JEDLICKI E. A Lux-like quorum sensing system in the extreme acidophile Acidithiobacillus ferrooxidans. Biol. Res. 38, 283, 2005.
30. RUIZ L.M., VALENZUELA S., CASTRO M., GONZALEZ A., FREZZA M., SOULÈRE, L., ROHWERDER T., QUENEAU Y., DOUTHEAU A., SAND W., JEREZ C.A., GUILIANI N. AHL communication is a widespread phenomenon in biomining bacteria and seems to be involved in mineraladhesion efficiency. Hydrometallurgy 94, 133, 2008.
31. MUTSCHLER H., GEBHARDT M., SHOEMAN R.L., MEINHART A. A novel mechanism of programmed cell death in bacteria by toxin-antitoxin systems corrupts peptidoglycan synthesis. PLoS Biol. 9, (3), e1001033, 2011.
32. CASTONGUAY M.H., VAN DER SCHAAF S., KOESTER W., KROONEMAN J., VAN DER MEER W., HARMSEN H., LANDINI P. Biofilm formation by Escherichia coli is stimulated by synergistic interactions and co-adhesion mechanisms with adherence-proficient bacteria. Res. Microbiol. 157, (5), 471, 2006.
33. HARRISON J.J., CERI H., TURNER R.J. Multiple metal resistance and tolerance in microbial biofilms. Nat. Rev. Microbiol. 5, 928, 2007.
34. HOFFMAN L.R., D'ARGENIO D.A., MACCOSS M.J., ZHANG Z., JONES R.A., MILLER S.I. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436, (7054), 1171, 2005.
35. CHEN Y., CAO S., CHAI Y., CLARDY J., KOLTER R., GUO J.H., LOSICK R. A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants. Mol. Microbiol. 85, (3), 418, 2012.
36. PÉREZ-GIMÉNEZ J., MONGIARDINI E.J., ALTHABEGOITI M.J., COVELLI J., QUELAS J.I., LÓPEZ-GARCÍA S.L., LODEIRO A.R. Soybean lectin enhances biofilm formation by Bradyrhizobium japonicum in the absence of plants. Int. J. Microbiol. 719367, 2009.
37. BELOIN C., VALLE J., LATOUR-LAMBERT P., FAURE P., KRZEMINSKI P., BALESTRINO D., HAAGENSEN J.A., MOLIN S., PRENSIER G., Arbeille B., Ghigo J.M. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol. Microbiol. 51, (3), 659, 2004.
38. SAUER K., CAMPER A.K. Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J. Bacteriol. 183, (22), 6579, 2001.
39. WHITCHURCH C.B., TOLKER-NIELSEN T., RAGAS P.C., MATTICK J.S. Extracellular DNA required for bacterial biofilm formation. Science 295, (5559), 1487, 2002.
40. CALDWELL D.E. The calculative nature of microbial biofilms and bioaggregates. Int. Microbiol. 5, 107, 2002.
41. WANG X., ROCHON M., LAMPROKOSTOPOULOU A., LÜNSDORF H., NIMTZ M., RÖMLING U. Impact of biofilm matrix components on interaction of commensal Escherichia coli with the gastrointestinal cell line HT-29. Cell Mol. Life Sci. 63, (19-20), 2352, 2006.
42. WHITE A.P., GIBSON D.L., KIM W., KAY W.W., SURETTE M.G., Thin aggregative fimbriae and cellulose enhance long-term survival and persistence of Salmonella. J. Bacteriol. 188, (9), 3219, 2006.
43. GHIGO J.M. Are there biofilm-specific physiological pathways beyond a reasonable doubt? Res. Microbiol. 154, (1), 1, 2003.
44. SCHUSTER M., HAWKINS A.C., HARWOOD C.S., GREENBERG E.P. The Pseudomonas aeruginosa RpoS regulon and its relationship to quorum sensing. Mol. Microbiol. 51, 973, 2004.
45. VAN DELDEN C., COMTE R., BALLY A.M. Stringent response activates quorum sensing and modulates cell density-dependent gene expression in Pseudomonas aeruginosa. J. Bacteriol. 183, (18), 5376, 2001.
46. SCHEMBRI M.A., KJAERGAARD K., KLEMM P. Global gene expression in Escherichia coli biofilms. Mol. Microbiol. 48, (1), 253, 2003.
47. TAYLOR C.M., BERESFORD M., EPTON H.A., SIGEE D.C., SHAMA G., ANDREW P.W., ROBERTS I.S. Listeria monocytogenes relA and hpt mutants are impaired in surface-attached growth and virulence. J. Bacteriol. 184, (3), 621, 2002.
48. BALZER G.J., MCLEAN R.J.C. The stringent response genes relA and spoT are important for Escherichia coli biofilms under slow-growth conditions. Can. J. Microbiol. 48, 675, 2002.
49. PRIGENT-COMBARET C., BROMBACHER E., VIDAL O., AMBERT A., LEJEUNE P., LANDINI P., DOREL C. Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J. Bacteriol. 183, (24), 7213, 2001.
50. LACQUA A., WANNER O., COLANGELO T., MARTINOTTI M.G., AND LANDINI P. Emergence of biofilmforming subpopulations upon exposure of Escherichia coli to environmental bacteriophages. Appl. Environ. Microbiol. 72, (1), 956, 2006.
51. WEBB J.S., THOMPSON L.S., JAMES S., CHARLTON T., TOLKER-NIELSEN T., KOCH B., GIVSKOV M., KJELLEBERG S. Cell death in Pseudomonas aeruginosa biofilm development. J. Bacteriol. 185, (15), 4585, 2003.
52. ELKINS J.G., HASSETT D.J., STEWART P.S., SCHWEIZER H.P., MCDERMOTT T.R. Protective role of catalase in Pseudomonas aeruginosa biofilm resistance to hydrogen peroxide. Appl. Environ. Microbiol. 65, 4594, 1999.
53. ZHANG X.S., GARCÍA-CONTRERAS R., WOOD T.K. YcfR (BhsA) influences Escherichia coli biofilm formation through stress response and surface hydrophobicity. J. Bacteriol. 189, (8), 3051, 2007.
54. TEITZEL G.M., PARSEK M.R. Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl. Environ. Microbiol. 69, 2313, 2003.
55. COSTERTON J.W., STEWART P.S., GREENBERG E.P. Bacterial biofilms: A common cause of persistent infections. Science 284, (5418), 1318, 1999.
56. OLIVER J.D. Viable but nonculturable bacteria in food environments. In: P.M. Fratamico and A.K. Bhunia (Eds.), Ford Borne Pathogens: Microbiology and Molecular Biology. Horizon Scientific Press, Norfolk, U.K. 2005.
57. COUTARD F., POMMEPUY M., LOAEC S., HERVIOHEATH D. mRNA detection by reverse transcription-PCR for monitoring viability and potential virulence in a pathogenic strain of Vibrio parahaemolyticus in viable but nonculturable state. J. Appl. Microbiol. 98, (4), 951, 2005.
58. ZHONG L., CHEN J., ZHANG X.H., JIANG Y.A. Entry of Vibrio cincinnatiensis into viable but nonculturable state and its resuscitation. Lett. Appl. Microbiol. 48, (2), 247, 2009.
59. NILSSON L., OLIVER J.D., KJELLEBERG S. Resuscitation of Vibrio vulnificus from the viable but nonculturable state. J. Bacteriol. 173, (16), 5054, 1991.
60. NARIYA H., INOUYE M. MazF, an mRNA interferase, mediates programmed cell death during multicellular Myxococcus development. Cell 132, (1), 55, 2008.
61. LI S., LEE B.U., SHIMKETS L.J. CsgA expression entrains Myxococcus xanthus development. Genes Dev. 6, (3), 401, 1992.
62. LOBEDANZ S., SØGAARD-ANDERSEN L. Identification of the C-signal, a contact-dependent morphogen coordinating multiple developmental responses in Myxococcus xanthus. Genes Dev. 17, 2151, 2003.
63. HARRIS B.Z., KAISER D., SINGER M. The guanosine nucleotide (p)ppGpp initiates development and A-factor production in myxococcus xanthus. Genes Dev. 12, (7), 1022, 1998.
64. MARTÍNEZ-GARCÍA E., TORMO A., NAVARROLLORÉNS J.M. GASP phenotype: presence in enterobacteria and independence of sigmaS in its acquisition. FEMS Microbiol. Lett. 225, (2), 201, 2003.
65. FINKEL S.E., ZINSER E., KOLTER R. Long-term survival and evolution in stationary phase. Bacterial Stress Responsem. ASM Press, Washington DC, pp. 231-238, 2000.
66. ZAMBRANO M.M., SIEGELE D.A., ALMIRÓN M., TORMO A., KOLTER R. Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259, (5102), 1757, 1993.
67. ROZEN D.E., PHILIPPE N., ARJAN DE VISSER J., LENSKI R.E., SCHNEIDER D. Death and cannibalism in a seasonal environment facilitate bacterial coexistence. Ecol. Lett. 12, (1), 34, 2009.
68. FARRELL M.J., FINKEL S.E. The growth advantage in stationary-phase phenotype conferred by rpoS mutations is dependent on the pH and nutrient environment. J. Bacteriol. 185, (24), 7044, 2003.
69. LEMONNIER M., LEVIN B.R., ROMEO T., GARNER K., BAQUERO M.-R., MERCANTE J., LEMICHEZ E., BAQUERO F., BLÁZQUEZ J. The evolution of contactdependent inhibition in non-growing populations of Escherichia coli. Proc. Biol. Sci. 275, (1630), 3, 2008.
70. EYMANN C., MITTENHUBER G., HECKER M. The stringent response, sigmaH-dependent gene expression and sporulation in Bacillus subtilis. Mol. Gen. Genet. 264, (6), 913, 2001.
71. OCHI K. Metabolic initiation of differentiation and secondary metabolism by Streptomyces griseus: significance of the stringent response (ppGpp) and GTP content in relation to A factor. J. Bacteriol. 169, (8), 3608, 1987.
72. GOTTLIEB D. The production and role of antibiotics in soil. J. Antibiot. 29, (10), 987, 1976.
73. NANJWADE B.K., CHANDRASHEKHARA S., GOUDANAVAR P.S., SHAMAREZ A.M., MANVI M.V. Production of antibiotics from soil-isolated actinomycetes and evaluation of their antimicrobial activities. Trop. J. Pharmaceut. Res. 9, 373, 2010.
74. KÜMMERER K. Drugs In the environment emission of drags, diagnostic aids and disinfectants into wastewater by hospitals in relation to other sources-a review. Chemosphere 45, 957, 2001.
75. HAMSCHER G., SCZESNY S., HÖPER H., NAU H. Determination of persistent tetracycline residues in soil fertilized with liquid manure by high-performance liquid chromatography with electrospray ionization tandem mass spectrometry. Anal. Chem. 74, (7), 1509, 2002.
76. VAN GOOL S. Possible effect on the environment of antibiotic residues in animal manure. Tijdschr. Diergeneeskd. 118, (1), 8, 1993.
77. WINCKLER C., GRAFE A. Stoffeintrag durch Tierarzneimittel und pharmakologisch wirksame Futterzusatzstoffe unter besonderer Berücksichtigung von Tetrazyklinen. UBA-Texte 44/00, Berlin 2000.
78. MORITA Y., SOBEL M.L., POOLE K. Antibiotic inducibility of the MexXY multidrug efflux system of Pseudomonas aeruginosa: involvement of the antibiotic-inducible PA5471 gene product. J. Bacteriol. 188, (5), 1847, 2006.
79. DÖRR T., LEWIS K., VULIĆ M. SOS response induces persistence to fluoroquinolones in Escherichia coli. PLoS Genet. 5, (12), e1000760, 2009.
80. MACFARLANE E.L., KWASNICKA A., OCHS M.M., HANCOCK R.E. PhoP-PhoQ homologues in Pseudomonas aeruginosa regulate expression of the outer-membrane protein OprH and polymyxin B resistance. Mol. Microbiol. 34, 305, 1999.
81. GROISMAN E.A., KAYSER J., SONCINI F.C. Regulation of polymyxin resistance and adaptation to low-Mg2+ environments. J. Bacteriol. 179, (22), 7040, 1997.
82. LEWENZA S., FALSAFI R., BAINS M., ROHS P., STUPAK J., SPROTT G.D., HANCOCK R.E. The olsA gene mediates the synthesis of an ornithine lipid in Pseudomonas aeruginosa during growth under phosphatelimiting conditions, but is not involved in antimicrobial peptide susceptibility. FEMS Microbiol. Lett. 320, (2), 95, 2011.
83. VINELLA D., ALBRECHT C., CASHEL M., D'ARI R. Iron limitation induces SpoT-dependent accumulation of ppGpp in E. coli. Mol. Microbiol. 56, (4), 958, 2005.
84. ROSNER J.L., SLONCZEWSKI J.L. Dual regulation of inaA by the multiple antibiotic resistance (mar) and superoxide (soxRS) stress response systems of Escherichia coli. J. Bacteriol. 176, (20), 6262, 1994.
85. O'CONNOR K., ZUSMAN D. Induction of β-lactamase influences the course of development in Myxococcus xanthus. J. Bacteriol. 181, (20), 6319, 1999.
86. NGUYEN D., JOSHI-DATAR A., LEPINE F., BAUERLE E., OLAKANMI O., BEER K., MCKAY G., SIEHNEL R., SCHAFHAUSER J., WANG Y., BRITIGAN B.E., SINGH P.K. Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334, (6058), 982, 2011.
87. THOMSEN L.E., OLSEN J.E., FOSTER J.W., INGMER H. ClpP is involved in the stress response and degradation of misfolded proteins in Salmonella enterica serovar Typhimurium. Microbiology 148, 2727, 2002.
88. VAKULENKO S.B., MOBASHERY S. Versatility of aminoglycosides and prospects for their future. Clin. Microbiol. Rev. 16, (3), 430, 2003.
89. KUHAR I., ŽGUR-BERTOK D. Transcription regulation of the colicin K cka gene reveals induction of colicin synthesis by differential responses to environmental signals. J. Bacteriol. 181, (23), 7373, 1999.
90. HOYT S., JONES G.H. RelA is required for actinomycin production in Streptomyces antibioticus. J. Bacteriol. 181, (12), 3824, 1999.
91. KANG S.G., JIN W., BIBB M., LEE K.J. Actinorhodin and undecylprodigiosin production in wild-type and relA mutant strains of Streptomyces coelicolor A3(2) grown in continuous culture. FEMS Microbiol. Lett. 168, (2), 221, 1998.
92. EYDMANN T., SÖDERBÄCK E., JONES T., HILL S., AUSTIN S., DIXON R. Transcriptional activation of the nitrogenase promoter in vitro: adnenosine nucleotides are required for inhibition of NifA activity by NifL. J. Bacteriol. 177, (5), 1186, 1995.
93. VAN RHIJN P., VANDERLEYDEN J. The Rhizobiumplant symbiosis. Microbiol. Mol. Biol. Rev. 59, (1), 124, 1995.
94. ROTH E., JEON K., STACEY G. Homology in endosymbiotic systems: the term 'symbiosome'. In 'Molecular genetics of plant microbe interactions'. (Eds R Palacios and DPS Verma), 220-225. (American Phytopathology Society Press: St Paul, MN) 1988.
95. WELLS D.H., LONG S.R. The Sinorhizobium meliloti stringent response affects multiple aspects of symbiosis. Mol. Microbiol. 43, (5), 1115, 2002.
96. MORIS M., BRAEKEN K., SCHOETERS E., VERRETH C., BEULLENS S., VANDERLEYDEN J., MICHIELS J. Effective symbiosis between Rhizobium etli and Phaseolus vulgaris requires the alarmone ppGpp. J. Bacteriol. 187, (15), 5460, 2005.
97. BRAEKEN K., FAUVART M., VERCRUYSSE M., BEULLENS S., LAMBRICHTS I., MICHIELS J. Pleiotropic effects of a rel mutation on stress survival of Rhizobium etli CNPAF512. BMC Microbiol. 10, (8), 219, 2008.
98. CALDERÓN-FLORES A., DU PONT G., HUERTASAQUERO A., MERCHANT-LARIOS H., SERVÍNGONZÁLEZ L., DÚRAN S. The stringent response is required for amino acid and nitrate utilization, Nod factor regulation, nodulation and nitrogen fixation in Rhizobium etli. J. Bacteriol. 187, (15), 5075, 2005.
99. SENEVIRATNE G., JAYASINGHEARACHCHI H.S. Mycelial colonization by bradyrhizobia and azorhizobia. J. Biosci. 28, (2), 243, 2003.
100. FUJISHIGE N.A., KAPADIA N.N., DE HOFF P.L., HIRSCH A.M. Investigations of Rhizobium biofilm formation. FEMS Microbiol. Ecol. 56, (2), 195, 2006.
101. HOWORTH M., ENGLAND R.R. Accumulation of ppGpp in symbiotic and free-living nitrogen-fixing bacteria following amino acid starvation. Arch. Microbiol. 171, 131, 1999.
102. SANDERCOCK J.R., PAGE W.J. RpoS expression and the general stress response in Azotobacter vinelandii during carbon and nitrogen diauxic shifts. J. Bacteriol. 190, (3), 946, 2008.
103. OLSÉN A., JONSSON A., NORMARK S. Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338, (6217), 652, 1989.