1887

Abstract

Alphaproteobacteria belonging to the group of the sphingomonads are frequently found in biofilms colonizing pure-water systems, where they cause technical and hygienic problems. In this study, physiological properties of sphingomonads for biofilm formation on plastic surfaces were analysed. sp. strain S2M10 was isolated from a used water-filtration membrane and submitted to transposon mutagenesis for isolating mutants with altered biofilm formation. Mutants showing strongly decreased biofilm formation carried transposon insertions in genes for the biosynthesis of the polysaccharide sphingan and for flagellar motility. Flagella-mediated attachment was apparently important for biofilm formation on plastic materials of intermediate hydrophobicity, while a mutant with defect in , encoding the first enzyme in sphingan biosynthesis, showed no biofilm formation on all tested materials. Sphingan-dependent biofilm formation was induced in the presence of specific carbon sources while it was not induced in complex medium with yeast extract and tryptone. The regulation of sphingan-based biofilm formation was investigated by interfering with the CckA/ChpT/CtrA phosphorelay, a central signal-transduction pathway in most Alphaproteobacteria. Construction and ectopic expression of a kinase-deficient histidine kinase CckA caused cell elongation and massive sphingan-dependent cell aggregation. In addition, it caused increased activity of the promotor of . In conclusion, these results indicate that sphingan-based biofilm formation by sphingomonads might be triggered by specific carbon sources under prototrophic conditions resembling a milieu that often prevails in pure-water systems.

Keyword(s): biofilm , CckA , GelA , plastic , sphingan and Sphingomonas
Funding
This study was supported by the:
  • Niedersächsische Staatskanzlei (Award 142078)
    • Principle Award Recipient: Bodo Philipp
  • Ministerie van Economische Zaken (Award 142078)
    • Principle Award Recipient: Bodo Philipp
  • Ministerium für Innovation, Wissenschaft und Forschung des Landes Nordrhein-Westfalen (Award 142078)
    • Principle Award Recipient: Bodo Philipp
  • EFRE (Award 142078)
    • Principle Award Recipient: Bodo Philipp
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2020-08-07
2024-04-25
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References

  1. Wingender J, Flemming H-C. Biofilms in drinking water and their role as reservoir for pathogens. Int J Hyg Environ Health 2011; 214:417–423 [View Article][PubMed]
    [Google Scholar]
  2. Tsao H-F, Scheikl U, Herbold C, Indra A, Walochnik J et al. The cooling tower water microbiota: seasonal dynamics and co-occurrence of bacterial and protist phylotypes. Water Res 2019; 159:464–479 [View Article][PubMed]
    [Google Scholar]
  3. Falkinham JO. Common features of opportunistic premise plumbing pathogens. Int J Environ Res Public Health 2015; 12:4533–4545 [View Article][PubMed]
    [Google Scholar]
  4. Popp N, Schlömann M, Mau M. Bacterial diversity in the active stage of a bioremediation system for mineral oil hydrocarbon-contaminated soils. Microbiology 2006; 152:3291–3304 [View Article][PubMed]
    [Google Scholar]
  5. Buonaurio R, Stravato VM, Kosako Y, Fujiwara N, Naka T et al. Sphingomonas melonis sp. nov., a novel pathogen that causes brown spots on yellow Spanish melon fruits. Int J Syst Evol Microbiol 2002; 52:2081–2087 [View Article][PubMed]
    [Google Scholar]
  6. Xie C-H, Yokota A. Sphingomonas azotifigens sp. nov., a nitrogen-fixing bacterium isolated from the roots of Oryza sativa. Int J Syst Evol Microbiol 2006; 56:889–893 [View Article][PubMed]
    [Google Scholar]
  7. Menon RR, Kumari S, Kumar P, Verma A, Krishnamurthi S et al. Sphingomonas pokkalii sp. nov., a novel plant associated rhizobacterium isolated from a saline tolerant pokkali rice and its draft genome analysis. Syst Appl Microbiol 2019; 42:334–342 [View Article][PubMed]
    [Google Scholar]
  8. Cavicchioli R, Fegatella F, Ostrowski M, Eguchi M, Gottschal J. Sphingomonads from marine environments. J Ind Microbiol Biotechnol 1999; 23:268–272 [View Article][PubMed]
    [Google Scholar]
  9. Jogler M, Siemens H, Chen H, Bunk B, Sikorski J et al. Identification and targeted cultivation of abundant novel freshwater sphingomonads and analysis of their population substructure. Appl Environ Microbiol 2011; 77:7355–7364 [View Article][PubMed]
    [Google Scholar]
  10. Vaz-Moreira I, Nunes OC, Manaia CM. Ubiquitous and persistent Proteobacteria and other Gram-negative bacteria in drinking water. Sci Total Environ 2017; 586:1141–1149 [View Article][PubMed]
    [Google Scholar]
  11. Chan S, Pullerits K, Keucken A, Persson KM, Paul CJ et al. Bacterial release from pipe biofilm in a full-scale drinking water distribution system. NPJ Biofilms Microbiomes 2019; 5:9 [View Article][PubMed]
    [Google Scholar]
  12. Pang CM, Hong P, Guo H, Liu W-T. Biofilm formation characteristics of bacterial isolates retrieved from a reverse osmosis membrane. Environ Sci Technol 2005; 39:7541–7550 [View Article][PubMed]
    [Google Scholar]
  13. Bereschenko LA, Stams AJM, Heilig GHJ, Euverink GJW, Nederlof MM et al. Investigation of microbial communities on reverse osmosis membranes used for process water production. Water Sci Technol 2007; 55:181–190 [View Article][PubMed]
    [Google Scholar]
  14. de Vries HJ, Beyer F, Jarzembowska M, Lipińska J, van den Brink P et al. Isolation and characterization of Sphingomonadaceae from fouled membranes. NPJ Biofilms Microbiomes 2019; 5:6 [View Article][PubMed]
    [Google Scholar]
  15. Bereschenko LA, Stams AJM, Euverink GJW, van Loosdrecht MCM. Biofilm formation on reverse osmosis membranes is initiated and dominated by Sphingomonas spp . Appl Environ Microbiol 2010; 76:2623–2632 [View Article][PubMed]
    [Google Scholar]
  16. de Vries HJ, Stams AJM, Plugge CM. Biodiversity and ecology of microorganisms in high pressure membrane filtration systems. Water Res 2020; 172:115511 [View Article][PubMed]
    [Google Scholar]
  17. Gutman J, Herzberg M, Walker SL. Biofouling of reverse osmosis membranes: positively contributing factors of Sphingomonas . Environ Sci Technol 2014; 48:13941–13950 [View Article][PubMed]
    [Google Scholar]
  18. Food Standards Agency Approved additives and E numbers: additives and E numbers for colours, preservatives, antioxidants, sweeteners, emulsifiers, stabilisers, thickeners and other types of additives; 2018
  19. Allen FL, Best GH, Lindroth TA. Welan Gum in Cement Compositions 4 US Patent; 1990 pp 963–668
    [Google Scholar]
  20. Osmałek T, Froelich A, Tasarek S. Application of gellan gum in pharmacy and medicine. Int J Pharm 2014; 466:328–340 [View Article][PubMed]
    [Google Scholar]
  21. Schmid J, Sperl N, Sieber V. A comparison of genes involved in sphingan biosynthesis brought up to date. Appl Microbiol Biotechnol 2014; 98:7719–7733 [View Article][PubMed]
    [Google Scholar]
  22. Azeredo J, Oliveira R. The Role of Exopolymers Produced by Sphingomonas paucimobilis in Biofilm Formation and Composition. Biofouling 2000; 16:17–27
    [Google Scholar]
  23. Harding NE, Patel YN, Coleman RJ. Organization of genes required for gellan polysaccharide biosynthesis in Sphingomonas elodea ATCC 31461. J Ind Microbiol Biotechnol 2004; 31:70–82 [View Article][PubMed]
    [Google Scholar]
  24. Jacobs C, Domian IJ, Maddock JR, Shapiro L. Cell cycle-dependent polar localization of an essential bacterial histidine kinase that controls DNA replication and cell division. Cell 1999; 97:111–120 [View Article][PubMed]
    [Google Scholar]
  25. Greene SE, Brilli M, Biondi EG, Komeili A. Analysis of the CtrA pathway in Magnetospirillum reveals an ancestral role in motility in alphaproteobacteria. J Bacteriol 2012; 194:2973–2986 [View Article][PubMed]
    [Google Scholar]
  26. Pini F, De Nisco NJ, Ferri L, Penterman J, Fioravanti A et al. Cell cycle control by the master regulator ctrA in Sinorhizobium meliloti . PLoS Genet 2015; 11:e1005232 [View Article][PubMed]
    [Google Scholar]
  27. Bellefontaine A-F, Pierreux CE, Mertens P, Vandenhaute J, Letesson J-J et al. Plasticity of a transcriptional regulation network among alpha-proteobacteria is supported by the identification of CtrA targets in Brucella abortus . Mol Microbiol 2002; 43:945–960 [View Article][PubMed]
    [Google Scholar]
  28. Lang AS, Beatty JT. Genetic analysis of a bacterial genetic exchange element: the gene transfer agent of Rhodobacter capsulatus . Proc Natl Acad Sci U S A 2000; 97:859–864 [View Article][PubMed]
    [Google Scholar]
  29. Francez-Charlot A, Kaczmarczyk A, Vorholt JA. The branched CcsA/CckA-ChpT-CtrA phosphorelay of Sphingomonas melonis controls motility and biofilm formation. Mol Microbiol 2015; 97:47–63 [View Article][PubMed]
    [Google Scholar]
  30. Wu M, Huang H, Li G, Ren Y, Shi Z et al. The evolutionary life cycle of the polysaccharide biosynthetic gene cluster based on the Sphingomonadaceae. Sci Rep 2017; 7:46484 [View Article][PubMed]
    [Google Scholar]
  31. Stolz A. Molecular characteristics of xenobiotic-degrading sphingomonads. Appl Microbiol Biotechnol 2009; 81:793–811 [View Article][PubMed]
    [Google Scholar]
  32. Bertani G, lysogenesis Son I. The mode of phage liberation by lysogenic Escherichia coli . J Bacteriol 1991; 62:293–300
    [Google Scholar]
  33. Klebensberger J, Rui O, Fritz E, Schink B, Philipp B. Cell aggregation of Pseudomonas aeruginosa strain PAO1 as an energy-dependent stress response during growth with sodium dodecyl sulfate. Arch Microbiol 2006; 185:417–427 [View Article][PubMed]
    [Google Scholar]
  34. Jagmann N, Brachvogel H-P, Philipp B. Parasitic growth of Pseudomonas aeruginosa in co-culture with the chitinolytic bacterium Aeromonas hydrophila . Environ Microbiol 2010; 12:1787–1802 [View Article][PubMed]
    [Google Scholar]
  35. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article][PubMed]
    [Google Scholar]
  36. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article][PubMed]
    [Google Scholar]
  37. García-Alcalde F, Okonechnikov K, Carbonell J, Cruz LM, Götz S et al. Qualimap: evaluating next-generation sequencing alignment data. Bioinformatics 2012; 28:2678–2679 [View Article][PubMed]
    [Google Scholar]
  38. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article][PubMed]
    [Google Scholar]
  39. Pilhofer M, Bauer AP, Schrallhammer M, Richter L, Ludwig W et al. Characterization of bacterial operons consisting of two tubulins and a kinesin-like gene by the novel two-step gene walking method. Nucleic Acids Res 2007; 35:e135 [View Article][PubMed]
    [Google Scholar]
  40. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA et al. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 1995; 166:175–176 [View Article][PubMed]
    [Google Scholar]
  41. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR. Site-Directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 1989; 77:51–59 [View Article][PubMed]
    [Google Scholar]
  42. Miller J. Experiments in Molecular Genetics Cold Spring Harbor Laboratory; 1972 pp 352–355
    [Google Scholar]
  43. Yamazaki M, Thorne L, Mikolajczak M, Armentrout RW, Pollock TJ. Linkage of genes essential for synthesis of a polysaccharide capsule in Sphingomonas strain S88. J Bacteriol 1996; 178:2676–2687 [View Article][PubMed]
    [Google Scholar]
  44. Bryan R, Purucker M, Gomes SL, Alexander W, Shapiro L. Analysis of the pleiotropic regulation of flagellar and chemotaxis gene expression in Caulobacter crescentus by using plasmid complementation. Proc Natl Acad Sci U S A 1984; 81:1341–1345 [View Article][PubMed]
    [Google Scholar]
  45. Alexopoulos JA, Guarné A, Ortega J. Clpp: a structurally dynamic protease regulated by AAA+ proteins. J Struct Biol 2012; 179:202–210 [View Article][PubMed]
    [Google Scholar]
  46. Diversified Enterprises Critical surface tension and contact angle with water for various polymers. 2020 Hompage of diversified Enterprises..
  47. Yücel O, Drees S, Jagmann N, Patschkowski T, Philipp B. An unexplored pathway for degradation of cholate requires a 7α-hydroxysteroid dehydratase and contributes to a broad metabolic repertoire for the utilization of bile salts in Novosphingobium sp. strain Chol11. Environ Microbiol 2016; 18:5187–5203 [View Article][PubMed]
    [Google Scholar]
  48. MacLellan SR, MacLean AM, Finan TM. Promoter prediction in the rhizobia. Microbiology 2006; 152:1751–1763 [View Article][PubMed]
    [Google Scholar]
  49. Mahajan A, Currie CG, Mackie S, Tree J, McAteer S et al. An investigation of the expression and adhesin function of H7 flagella in the interaction of Escherichia coli O157 : H7 with bovine intestinal epithelium. Cell Microbiol 2009; 11:121–137 [View Article][PubMed]
    [Google Scholar]
  50. Kawagishi I, Imagawa M, Imae Y, McCarter L, Homma M. The sodium-driven polar flagellar motor of marine Vibrio as the mechanosensor that regulates lateral flagellar expression. Mol Microbiol 1996; 20:693–699 [View Article][PubMed]
    [Google Scholar]
  51. Salta M, Wharton JA, Stoodley P, Dennington SP, Goodes LR et al. Designing biomimetic antifouling surfaces. Philos Trans A Math Phys Eng Sci 2010; 368:4729–4754 [View Article][PubMed]
    [Google Scholar]
  52. Jenal U. Signal transduction mechanisms in Caulobacter crescentus development and cell cycle control. FEMS Microbiol Rev 2000; 24:177–191 [View Article][PubMed]
    [Google Scholar]
  53. Mercer RG, Callister SJ, Lipton MS, Pasa-Tolic L, Strnad H et al. Loss of the response regulator CtrA causes pleiotropic effects on gene expression but does not affect growth phase regulation in Rhodobacter capsulatus . J Bacteriol 2010; 192:2701–2710 [View Article][PubMed]
    [Google Scholar]
  54. Liu C, Sun D, Zhu J, Liu W. Two-Component signal transduction systems: a major strategy for connecting input stimuli to biofilm formation. Front Microbiol 2018; 9:3279 [View Article][PubMed]
    [Google Scholar]
  55. Heindl JE, Crosby D, Brar S, Pinto JF, Singletary T et al. Reciprocal control of motility and biofilm formation by the PdhS2 two-component sensor kinase of Agrobacterium tumefaciens . Microbiology 2019; 165:146–162 [View Article][PubMed]
    [Google Scholar]
  56. Dubey BN, Lori C, Ozaki S, Fucile G, Plaza-Menacho I et al. Cyclic di-GMP mediates a histidine kinase/phosphatase switch by noncovalent domain cross-linking. Sci Adv 2016; 2:e1600823 [View Article][PubMed]
    [Google Scholar]
  57. Vega-Baray B, Domenzain C, Rivera A, Alfaro-López R, Gómez-César E et al. The flagellar set Fla2 in Rhodobacter sphaeroides is controlled by the CckA pathway and is repressed by organic acids and the expression of Fla1. J Bacteriol 2015; 197:833–847 [View Article][PubMed]
    [Google Scholar]
  58. Bergé M, Pezzatti J, González-Ruiz V, Degeorges L, Mottet-Osman G et al. Bacterial cell cycle control by citrate synthase independent of enzymatic activity. Elife 2020; 9:pii: e52272 [View Article][PubMed]
    [Google Scholar]
  59. Huang S, Voutchkov N, Jiang S, Carbon B. Balancing carbon, nitrogen and phosphorus concentration in seawater as a strategy to prevent accelerated membrane biofouling. Water Res 2019; 165:114978 [View Article][PubMed]
    [Google Scholar]
  60. Min KR, Rickard AH. Coaggregation by the freshwater bacterium Sphingomonas natatoria alters dual-species biofilm formation. Appl Environ Microbiol 2009; 75:3987–3997 [View Article][PubMed]
    [Google Scholar]
  61. Sambrook J, Russell DW. Molecular Cloning: a Laboratory Manual, 3rd ed. Cold Spring Harbor Laboratory Press; 2001
    [Google Scholar]
  62. Thoma S, Schobert M. An improved Escherichia coli donor strain for diparental mating. FEMS Microbiol Lett 2009; 294:127–132 [View Article][PubMed]
    [Google Scholar]
  63. de Lorenzo de, Herrero M, Jakubzik U, Timmis KN. Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J Bacteriol 1990; 172:6568–6572 [View Article][PubMed]
    [Google Scholar]
  64. Notredame C, Higgins DG, Heringa J. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 2000; 302:205–217 [View Article][PubMed]
    [Google Scholar]
  65. Letunic I, Doerks T, Bork P. SMART: recent updates, new developments and status in 2015. Nucleic Acids Res 2015; 43:D257–260 [View Article][PubMed]
    [Google Scholar]
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