Facultative control of matrix production optimizes competitive fitness in Pseudomonas aeruginosa PA14 biofilm models

Applied and Environmental Microbiology

Volumn 81, Issue 24, 2015, Pages 8414-8426

  Madsen, Jonas S ^a,b   Lin, Yu Cheng ^a   Squyres, Georgia R ^a   Price Whelan, Alexa ^a   Torio, Ana de Santiago ^a   Song, Angela ^a   Cornell, William C ^a   Sørensen, Soren J ^b   Xavier, Joao B ^c   Dietrich, Lars E P ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; COMPETITION; PHASE INTERFACES;

AIR LIQUID INTERFACES; COMMUNITY STRUCTURES; COMPETITIVE ADVANTAGE; COMPETITIVE FITNESS; ELECTRON ACCEPTOR; MATRIX POLYSACCHARIDES; PSEUDOMONAS AERUGINOSA; RESOURCE LIMITATIONS;

BIOFILMS;

BACTERIUM; BIOFILM; COLONY; EXPERIMENTAL STUDY; MATRIX; PATHOGEN;

PSEUDOMONAS AERUGINOSA;

BACTERIAL POLYSACCHARIDE; BACTERIAL PROTEIN;

BIOFILM; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; ORGANISMAL INTERACTION; PHENOTYPE; PSEUDOMONAS AERUGINOSA;

BACTERIAL PROTEINS; BIOFILMS; GENE EXPRESSION REGULATION, BACTERIAL; MICROBIAL INTERACTIONS; PHENOTYPE; POLYSACCHARIDES, BACTERIAL; PSEUDOMONAS AERUGINOSA;

EID: 84949647850     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02628-15     Document Type: Article

References (61)

1. Lopez D, Vlamakis H, Kolter R. 2010. Biofilms. Cold Spring Harb Perspect Biol 2:a000398.
2. Lewis K. 2001. Riddle of biofilm resistance. Antimicrob Agents Chemother 45:999-1007. http://dx.doi.org/10.1128/AAC.45.4.999-1007.2001.
3. Recinos DA, Sekedat MD, Hernandez A, Cohen TS, Sakhtah H, Prince AS, Price-Whelan A, Dietrich LE. 2012. Redundant phenazine operons in Pseudomonas aeruginosa exhibit environment-dependent expression and differential roles in pathogenicity. Proc Natl Acad Sci U S A 109: 19420-19425. http://dx.doi.org/10.1073/pnas.1213901109.
4. Dietrich LE, Teal TK, Price-Whelan A, Newman DK. 2008. Redoxactive antibiotics control gene expression and community behavior in divergent bacteria. Science 321:1203-1206. http://dx.doi.org/10.1126/science.1160619.
5. Dietrich LE, Okegbe C, Price-Whelan A, Sakhtah H, Hunter RC, Newman DK. 2013. Bacterial community morphogenesis is intimately linked to the intracellular redox state. J Bacteriol 195:1371-1380. http://dx.doi.org/10.1128/JB.02273-12.
6. Kempes CP, Okegbe C, Mears-Clarke Z, Follows MJ, Dietrich LE. 2014. Morphological optimization for access to dual oxidants in biofilms. Proc Natl Acad Sci U S A 111:208-213. http://dx.doi.org/10.1073/pnas.1315521110.
7. Price-Whelan A, Dietrich LE, Newman DK. 2007. Pyocyanin alters redox homeostasis and carbon flux through central metabolic pathways in Pseudomonas aeruginosa PA14. J Bacteriol 189:6372-6381. http://dx.doi.org/10.1128/JB.00505-07.
8. Wang Y, Kern SE, Newman DK. 2010. Endogenous phenazine antibiotics promote anaerobic survival of Pseudomonas aeruginosa via extracellular electron transfer. J Bacteriol 192:365-369. http://dx.doi.org/10.1128/JB.01188-09.
9. Arai H. 2011. Regulation and function of versatile aerobic and anaerobic respiratory metabolism in Pseudomonas aeruginosa. Front Microbiol 2:103.
10. Friedman L, Kolter R. 2004. Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51:675-690.
11. Jennings LK, Storek KM, Ledvina HE, Coulon C, Marmont LS, Sadovskaya I, Secor PR, Tseng BS, Scian M, Filloux A, Wozniak DJ, Howell PL, Parsek MR. 2015. Pel is a cationic exopolysaccharide that cross-links extracellular DNA in the Pseudomonas aeruginosa biofilm matrix. Proc Natl Acad Sci U S A 112:11353-11358. http://dx.doi.org/10.1073/pnas.1503058112.
12. Franklin MJ, Nivens DE, Weadge JT, Howell PL. 2011. Biosynthesis of the Pseudomonas aeruginosa extracellular polysaccharides, alginate, Pel, and Psl. Front Microbiol 2:167.
13. Friedman L, Kolter R. 2004. Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J Bacteriol 186:4457-4465. http://dx.doi.org/10.1128/JB.186.14.4457-4465.2004.
14. Vasseur P, Vallet-Gely I, Soscia C, Genin S, Filloux A. 2005. The pel genes of the Pseudomonas aeruginosa PAK strain are involved at early and late stages of biofilm formation. Microbiology 151:985-997. http://dx.doi.org/10.1099/mic.0.27410-0.
15. Colvin KM, Gordon VD, Murakami K, Borlee BR, Wozniak DJ, Wong GC, Parsek MR. 2011. The pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa. PLoS Pathog 7:e1001264. http://dx.doi.org/10.1371/journal.ppat.1001264.
16. Colvin KM, Alnabelseya N, Baker P, Whitney JC, Howell PL, Parsek MR. 2013. PelA deacetylase activity is required for Pel polysaccharide synthesis in Pseudomonas aeruginosa. J Bacteriol 195:2329-2339. http://dx.doi.org/10.1128/JB.02150-12.
17. Yamamoto K, Arai H, Ishii M, Igarashi Y. 2011. Trade-off between oxygen and iron acquisition in bacterial cells at the air-liquid interface. FEMS Microbiol Ecol 77:83-94. http://dx.doi.org/10.1111/j.1574-6941.2011.01087.x.
18. Xavier JB, Foster KR. 2007. Cooperation and conflict in microbial biofilms. Proc Natl Acad Sci U S A 104:876-881. http://dx.doi.org/10.1073/pnas.0607651104.
19. Nadell CD, Xavier JB, Foster KR. 2009. The sociobiology of biofilms. FEMS Microbiol Rev 33:206-224. http://dx.doi.org/10.1111/j.1574-6976.2008.00150.x.
20. Hamilton WD. 1964. Genetical evolution of social behaviour I. J Theor Biol 7:1-16. http://dx.doi.org/10.1016/0022-5193(64)90038-4.
21. Nadell CD, Bassler BL. 2011. A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms. Proc Natl Acad Sci U S A 108:14181-14185. http://dx.doi.org/10.1073/pnas.1111147108.
22. Nadell CD, Drescher K, Wingreen NS, Bassler BL. 2015. Extracellular matrix structure governs invasion resistance in bacterial biofilms. ISME J 9:1700-1709. http://dx.doi.org/10.1038/ismej.2014.246.
23. Smith DR, Maestre-Reyna M, Lee G, Gerard H, Wang AH, Watnick PI. 2015. In situ proteolysis of the Vibrio cholerae matrix protein RbmA promotes biofilm recruitment. Proc Natl Acad Sci U S A 112:10491-10496. http://dx.doi.org/10.1073/pnas.1512424112.
24. van Gestel J, Weissing FJ, Kuipers OP, Kovacs AT. 2014. Density of founder cells affects spatial pattern formation and cooperation in Bacillus subtilis biofilms. ISME J 8:2069-2079. http://dx.doi.org/10.1038/ismej.2014.52.
25. Foster KR, Xavier JB. 2007. Cooperation: bridging ecology and sociobiology. Curr Biol 17:R319-R321. http://dx.doi.org/10.1016/j.cub.2007.03.005.
26. Rainey PB, Rainey K. 2003. Evolution of cooperation and conflict in experimental bacterial populations. Nature 425:72-74. http://dx.doi.org/10.1038/nature01906.
27. 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. http://dx.doi.org/10.1073/pnas.0407460101.
28. Workentine ML, Sibley CD, Glezerson B, Purighalla S, Norgaard-Gron JC, Parkins MD, Rabin HR, Surette MG. 2013. Phenotypic heterogeneity of Pseudomonas aeruginosa populations in a cystic fibrosis patient. PLoS One 8:e60225. http://dx.doi.org/10.1371/journal.pone.0060225.
29. Ashish A, Paterson S, Mowat E, Fothergill JL, Walshaw MJ, Winstanley C. 2013. Extensive diversification is a common feature of Pseudomonas aeruginosa populations during respiratory infections in cystic fibrosis. J Cyst Fibros 12:790-793. http://dx.doi.org/10.1016/j.jcf.2013.04.003.
30. Markussen T, Marvig RL, Gomez-Lozano M, Aanaes K, Burleigh AE, Hoiby N, Johansen HK, Molin S, Jelsbak L. 2014. Environmental heterogeneity drives within-host diversification and evolution of Pseudomonas aeruginosa. mBio 5:e01592-14. http://dx.doi.org/10.1128/mBio.01592-14.
31. Rodriguez-Rojas A, Oliver A, Blazquez J. 2012. Intrinsic and environmental mutagenesis drive diversification and persistence of Pseudomonas aeruginosa in chronic lung infections. J Infect Dis 205:121-127. http://dx.doi.org/10.1093/infdis/jir690.
32. 2 gradients drive the evolution of the Wrinkly Spreader. ISME J 5:665-673. http://dx.doi.org/10.1038/ismej.2010.156.
33. Shanks RM, Caiazza NC, Hinsa SM, Toutain CM, O'Toole GA. 2006. Saccharomyces cerevisiae-based molecular tool kit for manipulation of genes from gram-negative bacteria. Appl Environ Microbiol 72:5027-5036.http://dx.doi.org/10.1128/AEM.00682-06.
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. http://dx.doi.org/10.1111/j.1462-2920.2004.00605.x.
35. Ueda A, Wood TK. 2009. Connecting quorum sensing, c-di-GMP, pel polysaccharide, and biofilm formation in Pseudomonas aeruginosa through tyrosine phosphatase TpbA (PA3885). PLoS Pathog 5:e1000483. http://dx.doi.org/10.1371/journal.ppat.1000483.
36. Spiers AJ, Bohannon J, Gehrig SM, Rainey PB. 2003. Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol Microbiol 50:15-27. http://dx.doi.org/10.1046/j.1365-2958.2003.03670.x.
37. Okegbe C, Sakhtah H, Sekedat MD, Price-Whelan A, Dietrich LE. 2012. Redox eustress: roles for redox-active metabolites in bacterial signaling and behavior. Antioxid Redox Signal 16:658-667. http://dx.doi.org/10.1089/ars.2011.4249.
38. de Vargas Roditi L, Boyle KE, Xavier JB. 2013. Multilevel selection analysis of a microbial social trait. Mol Syst Biol 9:684.
39. Werner E, Roe F, Bugnicourt A, Franklin MJ, Heydorn A, Molin S, Pitts B, Stewart PS. 2004. Stratified growth in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 70:6188-6196. http://dx.doi.org/10.1128/AEM.70.10.6188-6196.2004.
40. Hallatschek O, Hersen P, Ramanathan S, Nelson DR. 2007. Genetic drift at expanding frontiers promotes gene segregation. Proc Natl Acad Sci U S A 104:19926-19930. http://dx.doi.org/10.1073/pnas.0710150104.
41. Schluter J, Nadell CD, Bassler BL, Foster KR. 2015. Adhesion as a weapon in microbial competition. ISME J 9:139-149. http://dx.doi.org/10.1038/ismej.2014.174.
42. Spiers AJ, Kahn SG, Bohannon J, Travisano M, Rainey PB. 2002. Adaptive divergence in experimental populations of Pseudomonas fluorescens. I. Genetic and phenotypic bases of wrinkly spreader fitness. Genetics 161:33-46.
43. 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. http://dx.doi.org/10.1128/AEM.71.8.4809-4821.2005.
44. McBain AJ. 2009. Chapter 4. In vitro biofilm models: an overview. Adv Appl Microbiol 69:99-132.
45. Serra DO, Richter AM, Hengge R. 2013. Cellulose as an architectural element in spatially structured Escherichia coli biofilms. J Bacteriol 195: 5540-5554. http://dx.doi.org/10.1128/JB.00946-13.
46. Ali A, Rashid MH, Karaolis DK. 2002. High-frequency rugose exopolysaccharide production by Vibrio cholerae. Appl Environ Microbiol 68: 5773-5778. http://dx.doi.org/10.1128/AEM.68.11.5773-5778.2002.
47. Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R. 2013. Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol 11:157-168. http://dx.doi.org/10.1038/nrmicro2960.
48. Fong JC, Yildiz FH. 2007. The rbmBCDEF gene cluster modulates development of rugose colony morphology and biofilm formation in Vibrio cholerae. J Bacteriol 189:2319-2330. http://dx.doi.org/10.1128/JB.01569-06.
49. Okegbe C, Price-Whelan A, Dietrich LE. 2014. Redox-driven regulation of microbial community morphogenesis. Curr Opin Microbiol 18:39-45. http://dx.doi.org/10.1016/j.mib.2014.01.006.
50. Kim W, Racimo F, Schluter J, Levy SB, Foster KR. 2014. Importance of positioning for microbial evolution. Proc Natl Acad Sci U S A 111:E1639-E1647. http://dx.doi.org/10.1073/pnas.1323632111.
51. Hay ID, Wang Y, Moradali MF, Rehman ZU, Rehm BH. 2014. Genetics and regulation of bacterial alginate production. Environ Microbiol 16: 2997-3011. http://dx.doi.org/10.1111/1462-2920.12389.
52. McElroy KE, Hui JG, Woo JK, Luk AW, Webb JS, Kjelleberg S, Rice SA, Thomas T. 2014. Strain-specific parallel evolution drives shortterm diversification during Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci U S A 111:E1419-E1427. http://dx.doi.org/10.1073/pnas.1314340111.
53. Levins R. 1968. Evolution in changing environments: some theoretical explorations. Princeton University Press, Princeton, NJ.
54. Boles BR, Singh PK. 2008. Endogenous oxidative stress produces diversity and adaptability in biofilm communities. Proc Natl Acad Sci U S A 105:12503-12508. http://dx.doi.org/10.1073/pnas.0801499105.
55. Foster KR. 2009. A defense of sociobiology. Cold Spring Harbor Symp Quant Biol 74:403-418. http://dx.doi.org/10.1101/sqb.2009.74.041.
56. West SA, Griffin AS, Gardner A, Diggle SP. 2006. Social evolution theory for microorganisms. Nat Rev Microbiol 4:597-607. http://dx.doi.org/10.1038/nrmicro1461.
57. Cowley ES, Kopf SH, LaRiviere A, Ziebis W, Newman DK. 2015. Pediatric cystic fibrosis sputum can be chemically dynamic, anoxic, and extremely reduced due to hydrogen sulfide formation. mBio 6:e00767-15. http://dx.doi.org/10.1128/mBio.00767-15.
58. Jorth P, Staudinger BJ, Wu X, Hisert KB, Hayden H, Garudathri J, Harding CL, Radey MC, Rezayat A, Bautista G, Berrington WR, Goddard AF, Zheng C, Angermeyer A, Brittnacher MJ, Kitzman J, Shendure J, Fligner CL, Mittler J, Aitken ML, Manoil C, Bruce JE, Yahr TL, Singh PK. 2015. Regional isolation drives bacterial diversification within cystic fibrosis lungs. Cell Host Microbe 18:307-319. http://dx.doi.org/10.1016/j.chom.2015.07.006.
59. Rahme LG, Stevens EJ, Wolfort SF, Shao J, Tompkins RG, Ausubel FM. 1995. Common virulence factors for bacterial pathogenicity in plants and animals. Science 268:1899-1902. http://dx.doi.org/10.1126/science.7604262.
60. Dietrich LE, Price-Whelan A, Petersen A, Whiteley M, Newman DK. 2006. The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol Microbiol 61: 1308-1321. http://dx.doi.org/10.1111/j.1365-2958.2006.05306.x.
61. Dehio C, Meyer M. 1997. Maintenance of broad-host-range incompatibility group P and group Q plasmids and transposition of Tn5 in Bartonella henselae following conjugal plasmid transfer from Escherichia coli. J Bacteriol 179:538-540.