1887

Microbiology Society logo

Volume 152, Issue 3

AggA is required for aggregation and increased biofilm formation of a hyper-aggregating mutant of MR-1 Free

Abstract

COAG, a hyper-aggregating mutant of MR-1, was isolated from a rifampicin-challenged culture. Compared to the wild-type, COAG exhibited increased biofilm formation on glass carrier material. The role of surface-located proteins in the process of COAG auto-aggregation was confirmed by different proteolytic treatments of the aggregates. All of the tested proteolytic enzymes resulted in deflocculation within 3 h of incubation. In order to examine the altered expression of outer-membrane proteins in COAG, membrane-enriched cell preparations were analysed by proteomics and the protein pattern was compared to that of MR-1. From the proteomics results, it was hypothesized that the agglutination protein AggA, associated with the secretion of a putative RTX protein, was involved in the hyper-aggregating phenotype. These results were confirmed with a DNA microarray study of COAG versus MR-1. An insertional mutation in the COAG locus resulted in loss of the hyper-aggregating properties and the increased biofilm-forming capability. The insertional mutation resulted in strongly decreased attachment during the initial stage of biofilm formation. By complementing this mutation with the vector pCM62, expressing the gene, this effect could be nullified and biofilm formation was restored to at least the level of the MR-1 wild-type.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): 2D, two-dimensional , AI, aggregation index and Rif, rifampicin
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28204-0
2006-03-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/3/721.html?itemId=/content/journal/micro/10.1099/mic.0.28204-0&mimeType=html&fmt=ahah

References

  1. Alexeyev M. F. 1999; The pKNOCK series of broad-host-range mobilizable suicide vectors for gene knockout and targeted DNA insertion into the chromosome of Gram-negative bacteria. Biotechniques 26:824–828
     [Google Scholar]
  2. Artsimovitch I, Patlan V, Sekine S. I, Vassylyeva M. N, Hosaka T, Ochi K, Yokoyama S, Vassylyev D. G. 2004; Structural basis for transcription regulation by alarmone ppGpp . Cell 117:299–310 [CrossRef]
     [Google Scholar]
  3. Bagge D, Hjelm M, Johansen C, Huber I, Grami L. 2001; Shewanella putrefaciens adhesion and biofilm formation on food processing surfaces. Appl Environ Microbiol 67:2319–2325 [CrossRef]
     [Google Scholar]
  4. Bechet M, Blondeau R. 2003; Factors associated with the adherence and biofilm formation by Aeromonas caviae on glass surfaces. J Appl Microbiol 94:1072–1078 [CrossRef]
     [Google Scholar]
  5. Bieber D, Ramer S. W, Wu C. Y, Murray W. J, Tobe T, Fernandez R, Schoolnik G. K. 1998; Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli . Science 280:2114–2118 [CrossRef]
     [Google Scholar]
  6. Bossier P, Top E. M, Huys G, Kersters K, Boonaert C. J. P, Rouxhet P. G, Verstraete W. 2000; Modification of the aggregation behaviour of the environmental Ralstonia eutropha -like strain AE815 is reflected by both surface hydrophobicity and amplified fragment length polymorphism (AFLP) patterns. Environ Microbiol 2:51–58 [CrossRef]
     [Google Scholar]
  7. Caccavo F, Schamberger P. C, Keiding K, Nielsen P. H. 1997; Role of hydrophobicity in adhesion of the dissimilatory Fe(III)-reducing bacterium Shewanella alga to amorphous Fe(III) oxide. Appl Environ Microbiol 63:3837–3843
     [Google Scholar]
  8. Chiavelli D. A, Marsh J. W, Taylor R. K. 2001; The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl Environ Microbiol 67:3220–3225 [CrossRef]
     [Google Scholar]
  9. Czeczulin J. R, Balepur S, Hicks S, Phillips A, Hall R, Kothary M. H, Navarro-Garcia F, Nataro J. P. 1997; Aggregative adherence fimbria II, a second fimbrial antigen mediating aggregative adherence in enteroaggregative Escherichia coli . Infect Immun 65:4135–4145
     [Google Scholar]
  10. De Vriendt K, Theunissen S, Carpentier W, De Smet L, Devreese B, Van Beeumen J. 2005; Proteomics of Shewanella oneidensis MR-1 biofilm reveals differentially expressed proteins, including AggA and RibB. Proteomics 5:1308–1316 [CrossRef]
     [Google Scholar]
  11. Dubiel M, Hsu C. H, Chien C. C, Mansfeld F, Newman D. K. 2002; Microbial iron respiration can protect steel from corrosion. Appl Environ Microbiol 68:1440–1445 [CrossRef]
     [Google Scholar]
  12. Espinosa-Urgel M, Salido A, Ramos J. L. 2000; Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J Bacteriol 182:2363–2369 [CrossRef]
     [Google Scholar]
  13. Farrell A, Quilty B. 2002; Substrate-dependent autoaggregation of Pseudomonas putida CP1 during the degradation of mono-chlorophenols and phenol. J Ind Microbiol Biotechnol 28:316–324 [CrossRef]
     [Google Scholar]
  14. Gao H, Wang S, Liu X, Yan T, Wu L, Alm E, Arkin A, Thompson D. K, Zhou J. 2004; Global transcriptome analysis of the heat shock response of Shewanella oneidensis . J Bacteriol 186:7796–7803 [CrossRef]
     [Google Scholar]
  15. Hegde P, Qi R, Abernathy K. 7 other authors 2000; A concise guide to cDNA microarray analysis. Biotechniques 29:548–562
     [Google Scholar]
  16. Heidelberg J. F, Paulsen I. T, Nelson K. E. 40 other authors 2002; Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis . Nat Biotechnol 20:1118–1123 [CrossRef]
     [Google Scholar]
  17. Hinsa S. M, Espinosa-Urgel M, Ramos J. L, O'Toole G. A. 2003; Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted protein. Mol Microbiol 49:905–918 [CrossRef]
     [Google Scholar]
  18. Lee A. K, Newman D. K. 2003; Microbial iron respiration: impacts on corrosion processes. Appl Microbiol Biotechnol 62:134–139 [CrossRef]
     [Google Scholar]
  19. Little B, Wagner P, Hart K, Ray R, Lavoie D, Nealson K, Aguilar C. 1998; The role of biomineralization in microbiologically influenced corrosion. Biodegradation 9:1–10 [CrossRef]
     [Google Scholar]
  20. Lower S. K, Hochella M. F, Beveridge T. J. 2001; Bacterial recognition of mineral surfaces: nanoscale interactions between Shewanella and α -FeOOH. Science 292:1360–1363 [CrossRef]
     [Google Scholar]
  21. Malik A, Kakii K. 2003; Intergeneric coaggregations among Oligotropha carboxidovorans and Acinetobacter species present in activated sludge. FEMS Microbiol Lett 224:23–28 [CrossRef]
     [Google Scholar]
  22. Malik A, Sakamoto M, Ono T, Kakii K. 2003; Coaggregation between Acinetobacter johnsonii S35 and Microbacterium esteraromaticum strains isolated from sewage activated sludge. J Biosci Bioeng 96:10–15 [CrossRef]
     [Google Scholar]
  23. Marx C. J, Lidstrom M. E. 2001; Development of improved versatile broad-host-range vectors for use in methylotrophs and other Gram-negative bacteria. Microbiology 147:2065–2075
     [Google Scholar]
  24. Molloy M. P, Herbert B. R, Walsh B. J, Tyler M. I, Traini M, Sanchez J. C, Hochstrasser D. F, Williams K. L, Gooley A. A. 1998; Extraction of membrane proteins by differential solubilization for separation using two-dimensional gel electrophoresis. Electrophoresis 19:837–844 [CrossRef]
     [Google Scholar]
  25. Nataro J. P, Deng Y. K, Giron J. A, Savarino S. J, Kothary M. H, Hall R. 1993; Aggregative adherence fimbria-I expression in enteroaggregative Escherichia coli requires two unlinked plasmid regions. Infect Immun 61:1126–1131
     [Google Scholar]
  26. Olsen A, Jonsson A, Normark S. 1989; Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli . Nature 338:652–655 [CrossRef]
     [Google Scholar]
  27. O'Toole G, Kaplan H. B, Kolter R. 2000; Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79 [CrossRef]
     [Google Scholar]
  28. Sambrook J, Russell D. W. 2001 Molecular Cloning: a Laboratory Manual, 3rd edn.. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  29. Schembri M. A, Christiansen G, Klemm P. 2001; FimH-mediated autoaggregation of Escherichia coli . Mol Microbiol 41:1419–1430 [CrossRef]
     [Google Scholar]
  30. Schembri M. A, Hjerrild L, Gjermansen M, Klemm P. 2003a; Differential expression of the Escherichia coli autoaggregation factor antigen 43. J Bacteriol 185:2236–2242 [CrossRef]
     [Google Scholar]
  31. Schembri M. A, Kjaergaard K, Klemm P. 2003b; Global gene expression in Escherichia coli biofilms. Mol Microbiol 48:253–267 [CrossRef]
     [Google Scholar]
  32. Schena M, Shalon D, Heller R, Chai A, Brown P. O, Davis R. W. 1996; Parallel human genome analysis: microarray-based expression monitoring of 1000 genes. Proc Natl Acad Sci U S A 93:10614–10619 [CrossRef]
     [Google Scholar]
  33. Schreiber W, Stone K. D, Strong M. A, DeTolla L. J, Hoppert M, Donnenberg M. S. 2002; BfpU, a soluble protein essential for type IV pilus biogenesis in enteropathogenic Escherichia coli . Microbiology 148:2507–2518
     [Google Scholar]
  34. Semple K. M, Westlake D. W. S. 1987; Characterization of iron-reducing Alteromonas putrefaciens strains from oil field fluids. Can J Microbiol 33:366–371 [CrossRef]
     [Google Scholar]
  35. Thompson D. K, Beliaev A. S, Giometti C. S. 9 other authors 2002; Transcriptional and proteomic analysis of a ferric uptake regulator (fur) mutant of Shewanella oneidensis : Possible involvement of fur in energy metabolism, transcriptional regulation, and oxidative stress. Appl Environ Microbiol 68:1419–1430
     [Google Scholar]
  36. Thormann K. M, Saville R. M, Shukla S, Pelletier D. A, Spormann A. M. 2004; Initial phases of biofilm formation in Shewanella oneidensis MR-1. J Bacteriol 186:8096–8104 [CrossRef]
     [Google Scholar]
  37. Thormann K. M, Saville R. M, Shukla S, Spormann A. M. 2005; Induction of rapid detachment in Shewanella oneidensis MR-1 biofilms. J Bacteriol 187:1014–1021 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28204-0
Loading
AggA is required for aggregation and increased biofilm formation of a hyper-aggregating mutant of Shewanella oneidensis MR-1
Microbiology 152, 721 (2006); https://doi.org/10.1099/mic.0.28204-0
/content/journal/micro/10.1099/mic.0.28204-0
/content/journal/micro/10.1099/mic.0.28204-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

PDF

Supplementary material 3

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error