Exposure to solute stress affects genome-wide expression but not the polycyclic aromatic hydrocarbon-degrading activity of Sphingomonas sp. Strain LH128 in biofilms

Applied and Environmental Microbiology

Volumn 78, Issue 23, 2012, Pages 8311-8320

  Fida, Tekle Tafese ^a   Breugelmans, Philip ^a   Lavigne, Rob ^a   Coronado, Edith ^b   Johnson, David R ^b   Van Der Meer, Jan Roelof ^b   Mayer, Antonia P ^b   Heipieper, Hermann J ^c   Hofkens, Johan ^a   Springael, Dirk ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOFILM CELLS; CHRONIC STRESS; COMPATIBLE SOLUTES; DEGRADING ACTIVITIES; ION HOMEOSTASIS; IONIC STRESS; NACL SOLUTION; OXYGEN CONSUMPTION; PHENANTHRENE MINERALIZATION; POLYCYCLIC AROMATIC HYDROCARBONS(PAHS); POLYCYCLIC AROMATICS; PROTEIN SYNTHESIS; REGULATORY FUNCTIONS; SPHINGOMONAS; SPHINGOMONAS SP; STRESS FACTORS; STRESS RESPONSE;

ANTHRACENE; BIOCHEMISTRY; BIOFILMS; PHYSIOLOGICAL MODELS; PHYSIOLOGY; SODIUM CHLORIDE; TRANSCRIPTION;

GENE EXPRESSION REGULATION;

PHENANTHRENE; PHENANTHRENE DERIVATIVE; SODIUM CHLORIDE; TRANSCRIPTOME;

BACTERIUM; BIOFILM; CATALYST; GENE EXPRESSION; GENOME; MOTILITY; PAH; PHYSIOLOGICAL RESPONSE; SOLUTE;

ARTICLE; BIOFILM; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OSMOTIC PRESSURE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SPHINGOMONAS;

BIOFILMS; GENE EXPRESSION REGULATION, BACTERIAL; OSMOTIC PRESSURE; PHENANTHRENES; SALINE SOLUTION, HYPERTONIC; SPHINGOMONAS; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME;

SPHINGOMONAS; SPHINGOMONAS SP.;

EID: 84870796021     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02516-12     Document Type: Article

References (63)

1. Aspedon A, Palmer K, Whiteley M. 2006. Microarray analysis of the osmotic stress response in Pseudomonas aeruginosa. J. Bacteriol. 188: 2721-2725.
2. Bastiaens L, et al. 2000. Isolation of adherent polycyclic aromatic hydrocarbon (PAH)-degrading bacteria using PAH-sorbing carriers. Appl. Environ. Microbiol. 66:1834 -1843.
3. Beloin C, Ghigo JM. 2005. Finding gene-expression patterns in bacterial biofilms. Trends Microbiol. 13:16 -19.
4. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Stat. Methodol. 57:289 -300.
5. Besemer J, Borodovsky M. 2005. GeneMark: web software for gene finding in prokaryotes, eukaryotes, and viruses. Nucleic Acids Res. 33:W451- W454.
6. Beveridge TJ, Makin SA, Kadurugamuwa JL, Li Z. 1997. Interactions between biofilms and the environment. FEMS Microbiol. Rev. 20:291- 303.
7. Bligh EG, Dyer WJ. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917.
8. Brazma A, et al. 2001. Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat. Genet. 29: 365-371.
9. Busse MD, Bottomley PJ. 1989. Growth and nodulation responses of Rhizobium meliloti to water stress induced by permeating and nonpermeating solutes. Appl. Environ. Microbiol. 55:2431-2436.
10. Chang WS, Li X, Halverson LJ. 2009. Influence of water limitation on endogenous oxidative stress and cell death within unsaturated Pseudomonas putida biofilms. Environ. Microbiol. 11:1482-1492.
11. Conway T, Schoolnik GK. 2003. Microarray expression profiling: capturing a genome-wide portrait of the transcriptome. Mol. Microbiol. 47: 879-889.
12. Csonka LN. 1989. Physiological and genetic responses of bacteria to osmotic stress. Microbiol. Rev. 53:121-147.
13. Csonka LN, Ikeda TP, Fletcher SA, Kustu S. 1994. The accumulation of glutamate is necessary for optimal growth of Salmonella typhimurium in media of high osmolality but not induction of the proU operon. J. Bacteriol. 176:6324-6333.
14. Cytryn EJ, et al. 2007. Transcriptional and physiological responses of Bradyrhizobium japonicum to desiccation-induced stress. J. Bacteriol. 189: 6751-6762.
15. Dibrov P. 2005. The sodium cycle in Vibrio cholerae: riddles in the dark. Biochemistry (Mosc.) 70:150 -153.
16. Dominguez-Ferreras A, et al. 2006. Transcriptome profiling reveals the importance of plasmid pSymB for osmoadaptation of Sinorhizobium meliloti. J. Bacteriol. 188:7617-7625.
17. Domka J, Lee J, Bansal T, Wood TK. 2007. Temporal gene-expression in Escherichia coli K-12 biofilms. Environ. Microbiol. 9:332-346.
18. Edgar R, Domrachev M, Lash AE. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30:207-210.
19. Emerson WH, Jamieson DT. 1967. Some physical properties of sea water in various concentrations. Desalination 3:213-224.
20. Grimshaw JPA, Jelesarov I, Siegenthaler RK, Christen P. 2003. Thermosensor action of GrpE. J. Biol. Chem. 278:19048 -19053.
21. Hall-Stoodley L, Costerton JW, Stoodley P. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2:95-108.
22. Halverson LJ, Firestone MK. 2000. Differential effects of permeating and nonpermeating solutes on the fatty acid composition of Pseudomonas putida. Appl. Environ. Microbiol. 66:2414 -2421.
23. Hamilton S, et al. 2009. The transcriptional programme of Salmonella enterica serovar Typhimurium reveals a key role for tryptophan metabolism in biofilms. BMC Genomics 10:599. doi:10.1186/1471-2164-10-599.
24. Hancock V, Klemm P. 2007. Global gene expression profiling of asymptomatic bacteriuria Escherichia coli during biofilm growth in human urine. Infect. Immun. 75:966 -976.
25. He Z, et al. 2010. Global transcriptional, physiological, and metabolite analyses of the responses of Desulfovibrio vulgaris Hildenborough to salt adaptation. Appl. Environ. Microbiol. 76:1574 -1586.
26. Heipieper H, Neumann G, Cornelissen S, Meinhardt F. 2007. Solventtolerant bacteria for biotransformations in two-phase fermentation systems. Appl. Microbiol. Biotechnol. 74:961-973.
27. Heipieper HJ, Meulenbeld G, Van Oirschot Q, DeBont J. 1996. Effect of environmental factors on the trans/cis ratio of unsaturated fatty acids in Pseudomonas putida S12. Appl. Environ. Microbiol. 62:2773-2777.
28. Heydorn A, et al. 2000. Quantification of biofilm structures by the novel computer program Comstat. Microbiology 146:2395-2407.
29. Hoffmann T, Boiangiu C, Moses S, Bremer E. 2008. Responses of Bacillus subtilis to hypotonic challenges: physiological contributions of mechanosensitive channels to cellular survival. Appl. Environ. Microbiol. 74:2454 -2460.
30. Houry A, et al. 2012. Bacterial swimmers that infiltrate and take over the biofilm matrix. Proc. Natl. Acad. Sci. U. S. A. 109:13088 -13093.
31. Imlay JA. 2003. Pathways of oxidative damage. Annu. Rev. Microbiol. 57:395- 418.
32. Ishino F, et al. 1986. Peptidoglycan synthetic activities in membranes of Escherichia coli caused by overproduction of penicillin-binding protein 2 and rodA protein. J. Biol. Chem. 261:7024 -7031.
33. Jackson RB, Jobbäy EG. 2005. From icy roads to salty streams. Proc. Natl. Acad. Sci. U. S. A. 102:14487-14488.
34. Jebbar M, Sohn-Basser L, Bremer E, Bernard T, Blanco C. 2005. Ectoine-induced proteins in Sinorhizobium meliloti include an ectoine ABC-type transporter involved in osmoprotection and ectoine catabolism. J. Bacteriol. 187:1293-1304.
35. Jentsch TJ, Gunther W. 1997. Chloride channels: an emerging molecular picture. Bioessays 19:117-126.
36. Johnsen AR, et al. 2006. Microbial degradation of street dust polycyclic aromatic hydrocarbons in microcosms simulating diffuse pollution of urban soil. Environ. Microbiol. 8:535-545.
37. Johnsen AR, Wick LY, Harms H. 2005. Principles of microbial PAHdegradation in soil. Environ. Pollut. 133:71- 84.
38. Johnson D, Coronado E, Moreno-Forero S, Heipieper H, Van der Meer J. 2011. Transcriptome and membrane fatty acid analyses reveal different strategies for responding to permeating and non-permeating solutes in the bacterium Sphingomonas wittichii. BMC Microbiol. 11:250. doi:10.1186/ 1471-2180-11-250.
39. Leys NM, Ryngaert A, Bastiaens L, Verstraete W, Top EM, Springael D. 2004. Occurrence and phylogenetic diversity of Sphingomonas strains in soils contaminated with polycyclic aromatic hydrocarbons. Appl. Environ. Microbiol. 70:1944 -1955.
40. Liste H-H, Alexander M. 2000. Plant-promoted pyrene degradation in soil. Chemosphere 40:7-10.
41. Liu Y, et al. 2005. Transcriptome analysis of Shewanella oneidensis MR-1 in response to elevated salt conditions. J. Bacteriol. 187:2501-2507.
42. Mallick S, Chatterjee S, Dutta TK. 2007. A novel degradation pathway in the assimilation of phenanthrene by Staphylococcus sp. strain PN/Y via meta-cleavage of 2-hydroxy-1-naphthoic acid: formation of trans-2,3-dioxo-5-(2-hydroxyphenyl)-pent-4-enoic acid. Microbiology 153:2104- 2115.
43. Mantell A, Frenkel H, Meiri A. 1985. Drip irrigation of cotton with saline-sodic water. Irrig. Sci. 6:95-106.
44. Mrozik A, Piotrowska-Seget Z, Labuzek S. 2004. Cytoplasmatic bacterial membrane responses to environmental perturbations. Pol. J. Environ. Stud. 13:487- 494.
45. Nordberg EK. 2005. YODA: selecting signature oligonucleotides. Bioinformatics 21:1365-1370.
46. Papendick RI, Campbell GS. 1980. Theory and measurement of water potential, p 1-22. In Parr JF, Gardner WR, Elliott LF (ed), Water potential relations in soil microbiology. Soil Science Society of America, Madison, WI.
47. Raivio TL, Silhavy TJ. 2001. Periplasmic stress and ECF sigma factors. Annu. Rev. Microbiol. 55:591- 624.
48. Ramakrishna DM, Viraraghavan T. 2005. Environmental impact of chemical deicers: a review. Water Air Soil Pollut. 166:49-63.
49. Ramos JL, Marques S, Timmis KN. 1997. Transcriptional control of the Pseudomonas TOL plasmid catabolic operons is achieved through an interplay of host factors and plasmid-encoded regulators. Annu. Rev. Microbiol. 51:341-373.
50. Reasoner DJ, Geldreich EE. 1985. A new medium for the enumeration and subculture of bacteria from potable water. Appl. Environ. Microbiol. 49:1-7.
51. Record MT, Jr, Courtenay ES, Cayley DS, Guttman HJ. 1998. Responses of Escherichia coli to osmotic stress: large changes in amounts of cytoplasmic solutes and water. Trends Biochem. Sci. 23:143-148.
52. Shabala L, et al. 2009. Ion transport and osmotic adjustment in Escherichia coli in response to ionic and non-ionic osmotica. Environ. Microbiol. 11:137-148.
53. Shingler V. 1996. Signal sensing by sigma 54-dependent regulators: derepression as a control mechanism. Mol. Microbiol. 19:409-416.
54. Singh R, Paul D, Jain RK. 2006. Biofilms: implications in bioremediation. Trends Microbiol. 14:389 -397.
55. Stewart PS. 2003. Diffusion in biofilms. J. Bacteriol. 185:1485-1491.
56. Taglicht D, Padan E, Schuldiner S. 1991. Overproduction and purification of a functional Na /H antiporter coded by nhaA (ant) from Escherichia coli. J. Biol. Chem. 266:11289 -11294.
57. Tatusov RL, Koonin EV, Lipman DJ. 1997. A genomic perspective on protein families. Science 278:631- 637.
58. Tolker-Nielsen T, et al. 2000. Development and dynamics of Pseudomonas sp. biofilms. J. Bacteriol. 182:6482- 6489.
59. Uyttebroek M, Ortega-Calvo JJ, Breugelmans P, Springael D. 2006. Comparison of mineralization of solid-sorbed phenanthrene by polycyclic aromatic hydrocarbon (PAH)-degrading Mycobacterium spp. and Sphingomonas spp. Appl. Microbiol. Biotechnol. 72:829-836.
60. Waite RD, Papakonstantinopoulou A, Littler E, Curtis MA. 2005. Transcriptome analysis of Pseudomonas aeruginosa growth: comparison of gene expression in planktonic cultures and developing and mature biofilms. J. Bacteriol. 187:6571- 6576.
61. Welsh DT. 2000. Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol. Rev. 24:263-290.
62. White DC, Sutton SD, Ringelberg DB. 1996. The genus Sphingomonas: physiology and ecology. Curr. Opin. Biotechnol. 7:301-306.
63. Wouters K, et al. 2010. A non-invasive fluorescent staining procedure allows confocal laser scanning microscopy based imaging of Mycobacterium in multispecies biofilms colonizing and degrading polycyclic aromatic hydrocarbons. J. Microbiol. Methods 83:317-325.