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Emergence of a Synergistic Diversity as a Response to Competition in Pseudomonas putida Biofilms

  • Environmental Microbiology
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Abstract

Genetic diversification through the emergence of variants is one of the known mechanisms enabling the adaptation of bacterial communities. We focused in this work on the adaptation of the model strain Pseudomonas putida KT2440 in association with another P. putida strain (PCL1480) recently isolated from soil to investigate the potential role of bacterial interactions in the diversification process. On the basis of colony morphology, three variants of P. putida KT2440 were obtained from co-culture after 168 h of growth whereas no variant was identified from the axenic KT2440 biofilm. The variants exhibited distinct phenotypes and produced biofilms with specific architecture in comparison with the ancestor. The variants better competed with the P. putida PCL1480 strain in the dual-strain biofilms after 24 h of co-culture in comparison with the ancestor. Moreover, the synergistic interaction of KT2440 ancestor and the variants led to an improved biofilm production and to higher competitive ability versus the PCL1480 strain, highlighting the key role of diversification in the adaptation of P. putida KT2440 in the mixed community. Whole genome sequencing revealed mutations in polysaccharides biosynthesis protein, membrane transporter, or lipoprotein signal peptidase genes in variants.

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References

  1. Flemming HC, Wuertz S (2019) Bacteria and archaea on earth and their abundance in biofilms. Nat Rev Microbiol 17:247–260. https://doi.org/10.1038/s41579-019-0158-9

    Article  CAS  PubMed  Google Scholar 

  2. Hojo K, Nagaoka S, Ohshima T, Maeda N (2009) Bacterial interactions in dental biofilm development. J Dent Res 88:982–990. https://doi.org/10.1177/0022034509346811

    Article  CAS  PubMed  Google Scholar 

  3. Li YH, Tian X (2012) Quorum sensing and bacterial social interactions in biofilms. Sensors 12:2519–2538. https://doi.org/10.3390/s120302519

    Article  CAS  PubMed  Google Scholar 

  4. Bridier A, Briandet R, Bouchez T, Jabot F (2014) A model-based approach to detect interspecific interactions during biofilm development. Biofouling 30:761–771. https://doi.org/10.1080/08927014.2014.923409

    Article  PubMed  Google Scholar 

  5. Lykidis A, Chen CL, Tringe SG, McHardy AC, Copeland A, Kyrpides NC, Hugenholtz P, Macarie H, Olmos A, Monroy O, Liu WT (2011) Multiple syntrophic interactions in a terephthalate-degrading methanogenic consortium. ISME J 5:122–130. https://doi.org/10.1038/ismej.2010.125

    Article  CAS  PubMed  Google Scholar 

  6. Sieber JR, McInerney MJ, Gunsalus RP (2012) Genomic insights into syntrophy: the paradigm for anaerobic metabolic cooperation. Annu Rev Microbiol 66:429–452. https://doi.org/10.1146/annurev-micro-090110-102844

    Article  CAS  PubMed  Google Scholar 

  7. Kato S, Watanabe K (2010) Ecological and evolutionary interactions in syntrophic methanogenic consortia. Microbes Environ 25:145–151

    Article  Google Scholar 

  8. Ren D, Madsen JS, Sorensen SJ, Burmolle M (2014) High prevalence of biofilm synergy among bacterial soil isolates in cocultures indicates bacterial interspecific cooperation. ISME J. https://doi.org/10.1038/ismej.2014.96

  9. Bridier A, Sanchez-Vizuete Mdel P, Le Coq D, Aymerich S, Meylheuc T, Maillard JY, Thomas V, Dubois-Brissonnet F, Briandet R (2012) Biofilms of a Bacillus subtilis hospital isolate protect Staphylococcus aureus from biocide action. PLoS One 7:e44506. https://doi.org/10.1371/journal.pone.0044506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Lee KW, Periasamy S, Mukherjee M, Xie C, Kjelleberg S, Rice SA (2014) Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. ISME J 8:894–907. https://doi.org/10.1038/ismej.2013.194

    Article  CAS  PubMed  Google Scholar 

  11. Sanchez-Vizuete P, Le Coq D, Bridier A, Herry JM, Aymerich S, Briandet R (2015) Identification of ypqP as a new Bacillus subtilis biofilm determinant that mediates the protection of Staphylococcus aureus against antimicrobial agents in mixed-species communities. Appl Environ Microbiol 81:109–118. https://doi.org/10.1128/AEM.02473-14

    Article  CAS  PubMed  Google Scholar 

  12. Burmolle M, Ren D, Bjarnsholt T, Sorensen SJ (2014) Interactions in multispecies biofilms: do they actually matter? Trends Microbiol 22:84–91. https://doi.org/10.1016/j.tim.2013.12.004

    Article  CAS  PubMed  Google Scholar 

  13. Zhang QG, Buckling A, Ellis RJ, Godfray HC (2009) Coevolution between cooperators and cheats in a microbial system. Evolution 63:2248–2256. https://doi.org/10.1111/j.1558-5646.2009.00708.x

    Article  CAS  PubMed  Google Scholar 

  14. Bridier A, Piard JC, Pandin C, Labarthe S, Dubois-Brissonnet F, Briandet R (2017) Spatial organization plasticity as an adaptive driver of surface microbial communities. Front Microbiol 8:1364. https://doi.org/10.3389/fmicb.2017.01364

    Article  PubMed  PubMed Central  Google Scholar 

  15. McElroy KE, Hui JG, Woo JK, Luk AW, Webb JS, Kjelleberg S, Rice SA, Thomas T (2014) Strain-specific parallel evolution drives short-term diversification during Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci U S A 111:E1419–E1427. https://doi.org/10.1073/pnas.1314340111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Boles BR, Thoendel M, Singh PK (2004) Self-generated diversity produces “insurance effects” in biofilm communities. Proc Natl Acad Sci U S A 101:16630–16635. https://doi.org/10.1073/pnas.0407460101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Steenackers HP, Parijs I, Dubey A, Foster KR, Vanderleyden J (2016) Experimental evolution in biofilm populations. FEMS Microbiol Rev 40:373–397. https://doi.org/10.1093/femsre/fuw002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Martin M, Holscher T, Dragos A, Cooper VS, Kovacs AT (2016) Laboratory evolution of microbial interactions in bacterial biofilms. J Bacteriol 198:2564–2571. https://doi.org/10.1128/JB.01018-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Lujan AM, Macia MD, Yang L, Molin S, Oliver A, Smania AM (2011) Evolution and adaptation in Pseudomonas aeruginosa biofilms driven by mismatch repair system-deficient mutators. PLoS One 6:e27842. https://doi.org/10.1371/journal.pone.0027842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Allegrucci M, Sauer K (2007) Characterization of colony morphology variants isolated from Streptococcus pneumoniae biofilms. J Bacteriol 189:2030–2038. https://doi.org/10.1128/JB.01369-06

    Article  CAS  PubMed  Google Scholar 

  21. Yildiz FH, Schoolnik GK (1999) Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc Natl Acad Sci U S A 96:4028–4033

    Article  CAS  Google Scholar 

  22. Workentine ML, Harrison JJ, Weljie AM, Tran VA, Stenroos PU, Tremaroli V, Vogel HJ, Ceri H, Turner RJ (2010) Phenotypic and metabolic profiling of colony morphology variants evolved from Pseudomonas fluorescens biofilms. Environ Microbiol 12:1565–1577. https://doi.org/10.1111/j.1462-2920.2010.02185.x

    Article  CAS  PubMed  Google Scholar 

  23. Poltak SR, Cooper VS (2011) Ecological succession in long-term experimentally evolved biofilms produces synergistic communities. ISME J 5:369–378. https://doi.org/10.1038/ismej.2010.136

    Article  PubMed  Google Scholar 

  24. Ponciano JM, La HJ, Joyce P, Forney LJ (2009) Evolution of diversity in spatially structured Escherichia coli populations. Appl Environ Microbiol 75:6047–6054. https://doi.org/10.1128/AEM.00063-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Yarwood JM, Paquette KM, Tikh IB, Volper EM, Greenberg EP (2007) Generation of virulence factor variants in Staphylococcus aureus biofilms. J Bacteriol 189:7961–7967. https://doi.org/10.1128/JB.00789-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Traverse CC, Mayo-Smith LM, Poltak SR, Cooper VS (2013) Tangled bank of experimentally evolved Burkholderia biofilms reflects selection during chronic infections. Proc Natl Acad Sci U S A 110:E250–E259. https://doi.org/10.1073/pnas.1207025110

    Article  PubMed  Google Scholar 

  27. Starkey M, Hickman JH, Ma L, Zhang N, De Long S, Hinz A, Palacios S, Manoil C, Kirisits MJ, Starner TD, Wozniak DJ, Harwood CS, Parsek MR (2009) Pseudomonas aeruginosa rugose small-colony variants have adaptations that likely promote persistence in the cystic fibrosis lung. J Bacteriol 191:3492–3503. https://doi.org/10.1128/JB.00119-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Beyhan S, Bilecen K, Salama SR, Casper-Lindley C, Yildiz FH (2007) Regulation of rugosity and biofilm formation in Vibrio cholerae: comparison of VpsT and VpsR regulons and epistasis analysis of vpsT, vpsR, and hapR. J Bacteriol 189:388–402. https://doi.org/10.1128/JB.00981-06

    Article  CAS  PubMed  Google Scholar 

  29. Li W, Li Y, Wu Y, Cui Y, Liu Y, Shi X, Zhang Q, Chen Q, Sun Q, Hu Q (2016) Phenotypic and genetic changes in the life cycle of small colony variants of Salmonella enterica serotype Typhimurium induced by streptomycin. Ann Clin Microbiol Antimicrob 15:37–11. https://doi.org/10.1186/s12941-016-0151-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Lawrence D, Fiegna F, Behrends V, Bundy JG, Phillimore AB, Bell T, Barraclough TG (2012) Species interactions alter evolutionary responses to a novel environment. PLoS Biol 10:e1001330. https://doi.org/10.1371/journal.pbio.1001330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Hansen SK, Rainey PB, Haagensen JA, Molin S (2007) Evolution of species interactions in a biofilm community. Nature 445:533–536. https://doi.org/10.1038/nature05514

    Article  CAS  PubMed  Google Scholar 

  32. Freilich S, Zarecki R, Eilam O, Segal ES, Henry CS, Kupiec M, Gophna U, Sharan R, Ruppin E (2011) Competitive and cooperative metabolic interactions in bacterial communities. Nat Commun 2:589. https://doi.org/10.1038/Ncomms1597

    Article  PubMed  Google Scholar 

  33. Kuiper I, Lagendijk EL, Pickford R, Derrick JP, Lamers GE, Thomas-Oates JE, Lugtenberg BJ, Bloemberg GV (2004) Characterization of two Pseudomonas putida lipopeptide biosurfactants, putisolvin I and II, which inhibit biofilm formation and break down existing biofilms. Mol Microbiol 51:97–113

    Article  CAS  Google Scholar 

  34. Lambertsen L, Sternberg C, Molin S (2004) Mini-Tn7 transposons for site-specific tagging of bacteria with fluorescent proteins. Environ Microbiol 6:726–732. https://doi.org/10.1111/j.1462-2920.2004.00605.x

    Article  CAS  PubMed  Google Scholar 

  35. Lagendijk EL, Validov S, Lamers GEM, de Weert S, Bloemberg GV (2010) Genetic tools for tagging Gram-negative bacteria with mCherry for visualization in vitro and in natural habitats, biofilm and pathogenicity studies. FEMS Microbiol Lett 305:81–90. https://doi.org/10.1111/j.1574-6968.2010.01916.x

    Article  CAS  PubMed  Google Scholar 

  36. Weiss Nielsen M, Sternberg C, Molin S, Regenberg B (2011) Pseudomonas aeruginosa and Saccharomyces cerevisiae biofilm in flow cells. J Vis Exp 47:e2383. https://doi.org/10.3791/2383

    Article  CAS  Google Scholar 

  37. Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersboll BK, Molin S (2000) Quantification of biofilm structures by the novel computer program COMSTAT. Microbiol-Uk 146:2395–2407

    Article  CAS  Google Scholar 

  38. Rosenberg M, Gutnick D, Rosenberg E (1980) Adherence of bacteria to hydrocarbons-a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol Lett 9:29–33

    Article  CAS  Google Scholar 

  39. Cheroutre-Vialette M, Lebert I, Hebraud M, Labadie JC, Lebert A (1998) Effects of pH or a(w) stress on growth of Listeria monocytogenes. Int J Food Microbiol 42: 71-77.

  40. Lenski RE, Travisano M (1994) Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc Natl Acad Sci U S A 91:6808–6814

    Article  CAS  Google Scholar 

  41. Penterman J, Nguyen D, Anderson E, Staudinger BJ, Greenberg EP, Lam JS, Singh PK (2014) Rapid evolution of culture-impaired bacteria during adaptation to biofilm growth. Cell Rep 6:293–300. https://doi.org/10.1016/j.celrep.2013.12.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Flynn KM, Dowell G, Johnson TM, Koestler BJ, Waters CM, Cooper VS (2016) Evolution of ecological diversity in biofilms of Pseudomonas aeruginosa by altered cyclic diguanylate signaling. J Bacteriol 198:2608–2618. https://doi.org/10.1128/JB.00048-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Nelson KE, Weinel C, Paulsen IT, Dodson RJ, Hilbert H, Martins dos Santos VA, Fouts DE, Gill SR, Pop M, Holmes M, Brinkac L, Beanan M, DeBoy RT, Daugherty S, Kolonay J, Madupu R, Nelson W, White O, Peterson J, Khouri H, Hance I, Chris Lee P, Holtzapple E, Scanlan D, Tran K, Moazzez A, Utterback T, Rizzo M, Lee K, Kosack D, Moestl D, Wedler H, Lauber J, Stjepandic D, Hoheisel J, Straetz M, Heim S, Kiewitz C, Eisen JA, Timmis KN, Dusterhoft A, Tummler B, Fraser CM (2002) Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol 4:799–808

    Article  CAS  Google Scholar 

  44. Conibear TC, Collins SL, Webb JS (2009) Role of mutation in Pseudomonas aeruginosa biofilm development. PLoS One 4:e6289. https://doi.org/10.1371/journal.pone.0006289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Driffield K, Miller K, Bostock JM, O’Neill AJ, Chopra I (2008) Increased mutability of Pseudomonas aeruginosa in biofilms. J Antimicrob Chemother 61:1053–1056. https://doi.org/10.1093/jac/dkn044

    Article  CAS  PubMed  Google Scholar 

  46. Kelvin Lee KW, Hoong Yam JK, Mukherjee M, Periasamy S, Steinberg PD, Kjelleberg S, Rice SA (2016) Interspecific diversity reduces and functionally substitutes for intraspecific variation in biofilm communities. ISME J 10:846–857. https://doi.org/10.1038/ismej.2015.159

    Article  PubMed  Google Scholar 

  47. Koh KS, Lam KW, Alhede M, Queck SY, Labbate M, Kjelleberg S, Rice SA (2007) Phenotypic diversification and adaptation of Serratia marcescens MG1 biofilm-derived morphotypes. J Bacteriol 189:119–130. https://doi.org/10.1128/Jb.00930-06

    Article  CAS  PubMed  Google Scholar 

  48. Burrows LL, Urbanic RV, Lam JS (2000) Functional conservation of the polysaccharide biosynthetic protein WbpM and its homologues in Pseudomonas aeruginosa and other medically significant bacteria. Infect Immun 68:931–936. https://doi.org/10.1128/Iai.68.2.931-936.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Creuzenet C, Lam JS (2001) Topological and functional characterization of WbpM, an inner membrane UDP-GlcNAc C6 dehydratase essential for lipopolysaccharide biosynthesis in Pseudomonas aeruginosa. Mol Microbiol 41:1295–1310

    Article  CAS  Google Scholar 

  50. Hansen SK, Haagensen JAJ, Gjermansen M, Jorgensen TM, Tolker-Nielsen T, Molin S (2007) Characterization of a Pseudomonas putida rough variant evolved in a mixed-species biofilm with Acinetobacter sp strain C6. J Bacteriol 189:4932–4943. https://doi.org/10.1128/Jb.00041-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Lau PCY, Lindhout T, Beveridge TJ, Dutcher JR, Lam JS (2009) Differential lipopolysaccharide core capping leads to quantitative and correlated modifications of mechanical and structural properties in Pseudomonas aeruginosa biofilms. J Bacteriol 191:6618–6631. https://doi.org/10.1128/Jb.00698-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Kirisits MJ, Prost L, Starkey M, Parsek MR (2005) Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 71:4809–4821. https://doi.org/10.1128/AEM.71.8.4809-4821.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Lee YW, Jeong SY, In YH, Kim KY, So JS, Chang WS (2010) Lack of O-polysaccharide enhances biofilm formation by Bradyrhizobium japonicum. Lett Appl Microbiol 50:452–456. https://doi.org/10.1111/j.1472-765X.2010.02813.x

    Article  PubMed  Google Scholar 

  54. Prieto MA, Garcia JL (1997) Identification of the 4-hydroxyphenylacetate transport gene of Escherichia coli W: construction of a highly sensitive cellular biosensor. FEBS Lett 414:293–297

    Article  CAS  Google Scholar 

  55. Zhu X, Long F, Chen Y, Knochel S, She Q, Shi X (2008) A putative ABC transporter is involved in negative regulation of biofilm formation by Listeria monocytogenes. Appl Environ Microbiol 74:7675–7683. https://doi.org/10.1128/AEM.01229-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Hinsa SM, Espinosa-Urgel M, Ramos JL, O’Toole GA (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

    Article  CAS  Google Scholar 

  57. Wargnies B, Legrain C, Stalon V (1978) Anabolic ornithine carbamoyltransferase of Escherichia coli and catabolic ornithine carbamoyltransferase of Pseudomonas putida. Steady-state kinetic analysis. Eur J Biochem 89:203–212

    Article  CAS  Google Scholar 

  58. Falmagne P, Portetelle D, Stalon V (1985) Immunological and structural relatedness of catabolic ornithine carbamoyltransferases and the anabolic enzymes of enterobacteria. J Bacteriol 161:714–719

    Article  CAS  Google Scholar 

  59. Schurr MJ, Vickrey JF, Kumar AP, Campbell AL, Cunin R, Benjamin RC, Shanley MS, O’Donovan GA (1995) Aspartate transcarbamoylase genes of Pseudomonas putida: requirement for an inactive dihydroorotase for assembly into the dodecameric holoenzyme. J Bacteriol 177:1751–1759

    Article  CAS  Google Scholar 

  60. Yousef-Coronado F, Soriano MI, Yang L, Molin S, Espinosa-Urgel M (2011) Selection of hyperadherent mutants in Pseudomonas putida biofilms. Microbiology 157: 2257-2265. https://doi.org/10.1099/mic.0.047787-0

  61. Vasseur P, Soscia C, Voulhoux R, Filloux A (2007) PelC is a Pseudomonas aeruginosa outer membrane lipoprotein of the OMA family of proteins involved in exopolysaccharide transport. Biochimie 89:903–915. https://doi.org/10.1016/j.niochi.2007.04.002

    Article  CAS  PubMed  Google Scholar 

  62. Uhlich GA, Gunther NW, Bayles DO, Mosier DA (2009) The CsgA and Lpp proteins of an Escherichia coli O157:H7 strain affect HEp-2 cell invasion, motility, and biofilm formation. Infect Immun 77:1543–1552. https://doi.org/10.1128/Iai.00949-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Connelly MB, Young GA, Sloma A (2004) Extracellular proteolytic activity plays a central role in swarming motility in Bacillus subtilis. J Bacteriol 186:4159–4167. https://doi.org/10.1128/Jb.186.13.4159-4167.2004

    Article  CAS  PubMed  Google Scholar 

  64. Choi MH, Xu J, Gutierrez M, Yoo T, Cho YH, Yoon SC (2011) Metabolic relationship between polyhydroxyalkanoic acid and rhamnolipid synthesis in Pseudomonas aeruginosa: comparative (1)(3)C NMR analysis of the products in wild-type and mutants. J Biotechnol 151:30–42. https://doi.org/10.1016/j.jbiotec.2010.10.072

    Article  CAS  PubMed  Google Scholar 

  65. Wittgens A, Tiso T, Arndt TT, Wenk P, Hemmerich J, Muller C, Wichmann R, Kupper B, Zwick M, Wilhelm S, Hausmann R, Syldatk C, Rosenau F, Blank LM (2011) Growth independent rhamnolipid production from glucose using the non-pathogenic Pseudomonas putida KT2440. Microb Cell Factories 10:80. https://doi.org/10.1186/1475-2859-10-80

    Article  CAS  Google Scholar 

  66. Gutierrez M, Choi MH, Tian B, Xu J, Rho JK, Kim MO, Cho YH, Yoon SC (2013) Simultaneous inhibition of rhamnolipid and polyhydroxyalkanoic acid synthesis and biofilm formation in Pseudomonas aeruginosa by 2-bromoalkanoic acids: effect of inhibitor alkyl-chain-length. PloS One 8:e73986. https://doi.org/10.1371/journal.pone.0073986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Abdel-Mawgoud AM, Lepine F, Deziel E (2010) Rhamnolipids: diversity of structures, microbial origins and roles. Appl Microbiol Biotechnol 86:1323–1336. https://doi.org/10.1007/s00253-010-2498-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Davey ME, Caiazza NC, O’Toole GA (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185:1027–1036. https://doi.org/10.1128/Jb.185.3.1027-1036.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Boles BR, Thoendel M, Singh PK (2005) Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol Microbiol 57:1210–1223. https://doi.org/10.1111/j.1365-2958.2005.04743.x

    Article  CAS  PubMed  Google Scholar 

  70. Dusane DH, Nancharaiah YV, Zinjarde SS, Venugopalan VP (2010) Rhamnolipid mediated disruption of marine Bacillus pumilus biofilms. Colloid Surf B 81:242–248. https://doi.org/10.1016/j.colsurfb.2010.07.013

    Article  CAS  Google Scholar 

  71. Irie Y, O’Toole GA, Yuk MH (2005) Pseudomonas aeruginosa rhamnolipids disperse Bordetella bronchiseptica biofilms. FEMS Microbiol Lett 250:237–243. https://doi.org/10.1016/j.femsle.2005.07.012

    Article  CAS  PubMed  Google Scholar 

  72. Espinosa-Urgel M (2003) Resident parking only: rhamnolipids maintain fluid channels in biofilms. J Bacteriol 185:699–700. https://doi.org/10.1128/Jb.185.3.699-700.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Nemergut DR, Schmidt SK, Fukami T, O’Neill SP, Bilinski TM, Stanish LF, Knelman JE, Darcy JL, Lynch RC, Wickey P, Ferrenberg S (2013) Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev 77:342–356. https://doi.org/10.1128/MMBR.00051-12

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

Claus Sternberg is acknowledged for the kind gift of the P. putida KT2440 GFP strain and Ellen Lagendijk for the P.putida PCL1480 mCherry strain.

Funding

This work was funded by the French National Research Agency (ANR) within the SYSCOMM project DISCO (ANR-09-SYSC-003). This study was conducted on the LABE experimental platform funded by DRRT in the framework of CPER 2007–2013 projects.

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Correspondence to Arnaud Bridier.

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Bridier, A., Piard, J.C., Briandet, R. et al. Emergence of a Synergistic Diversity as a Response to Competition in Pseudomonas putida Biofilms. Microb Ecol 80, 47–59 (2020). https://doi.org/10.1007/s00248-019-01470-z

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