Pseudomonas aeruginosa PAO1 exopolysaccharides are important for mixed species biofilm community development and stress tolerance

Frontiers in Microbiology

Volumn 6, Issue AUG, 2015, Pages

  Periasamy, Saravanan ^a   Nair, Harikrishnan A S ^a,b   Lee, Kai W K ^a   Ong, Jolene ^a,c   Goh, Jie Q J ^a,c   Kjelleberg, Staffan ^a,c,d   Rice, Scott A ^a,c,d  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Biofilms; Exopolysaccharides; Interspecies competition; Mixed species consortia; Stress tolerance

Indexed keywords

ALGINIC ACID; EXOPOLYSACCHARIDE; PEL POLYSACCHARIDE; PSL POLYSACCHARIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIUM MUTANT; BIOFILM; ELECTROPORATION; FLOW CYTOMETRY; IMAGE ANALYSIS; MICROBIAL COMMUNITY; NONHUMAN; POLYMERASE CHAIN REACTION; PSEUDOMONAS AERUGINOSA; STRESS;

EID: 84940857668     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00851     Document Type: Article

References (39)

1. Barnes, R.J., Bandi, R.R., Chua, F., Low, J.H., Aung, T., Barraud, N., et al. (2014). The roles of Pseudomonas aeruginosa extracellular polysaccharides in biofouling of reverse osmosis membranes and nitric oxide induced dispersal. J. Mem. Sci. 466, 161-172. doi: 10.1016/j.memsci.2014.04.046.
2. Billings, N., Millan, M., Caldara, M., Rusconi, R., Tarasova, Y., Stocker, R., et al. (2013). The extracellular matrix component Psl provides fast-acting antibiotic defense in Pseudomonas aeruginosa biofilms. PLoS Pathog. 9:e1003526. doi: 10.1371/journal.ppat.1003526.
3. Campisano, A., Schroeder, C., Schemionek, M., Overhage, J., and Rehm, B.H. (2006). PslD is a secreted protein required for biofilm formation by Pseudomonas aeruginosa. Appl. Environ. Microbiol. 72, 3066-3068. doi: 10.1128/aem.72.4.3066-3068.2006.
4. Chew, S.C., Kundukad, B., Seviour, T., Van Der Maarel, J.R., Yang, L., Rice, S.A., et al. (2014). Dynamic remodeling of microbial biofilms by functionally distinct exopolysaccharides. MBio 5:e01536-14. doi: 10.1128/mBio.01536-14.
5. Choi, K.H., Gaynor, J.B., White, K.G., Lopez, C., Bosio, C.M., Karkhoff-Schweizer, R.R., et al. (2005). A Tn7-based broad-range bacterial cloning and expression system. Nat. Methods 2, 443-448. doi: 10.1038/nmeth765.
6. Choi, K.H., Kumar, A., and Schweizer, H.P. (2006). A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J. Microbiol. Methods 64, 391-397. doi: 10.1016/j.mimet.2005.06.001.
7. Colvin, K.M., Gordon, V.D., Murakami, K., Borlee, B.R., Wozniak, D.J., Wong, G.C., et al. (2011). The pel polysaccharide can serve a structural and protective role in the biofilm matrix of Pseudomonas aeruginosa. PLoS Pathog. 7:e1001264. doi: 10.1371/journal.ppat.1001264.
8. Colvin, K.M., Irie, Y., Tart, C.S., Urbano, R., Whitney, J.C., Ryder, C., et al. (2012). The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix. Environ. Microbiol. 14, 1913-1928. doi: 10.1111/j.1462-2920.2011.02657.x.
9. Costerton, J., Lewandowski, Z., Debeer, D., Caldwell, D., Korber, D., and James, G. (1994). Biofilms, the customized microniche. J. Bacteriol. 176, 2137-2142.
10. DeVault, J.D., Kimbara, K., and Chakrabarty, A.M. (1990). Pulmonary dehydration and infection in cystic fibrosis: evidence that ethanol activates alginate gene expression and induction of mucoidy in Pseudomonas aeruginosa. Mol. Microbiol. 4, 737-745. doi: 10.1111/j.1365-2958.1990.tb00644.x.
11. Folsom, J., Richards, L., Pitts, B., Roe, F., Ehrlich, G., Parker, A., et al. (2010). Physiology of Pseudomonas aeruginosa in biofilms as revealed by transcriptome analysis. BMC Microbiol. 10:294. doi: 10.1186/1471-2180-10-294.
12. Friedman, L., and Kolter, R. (2004). Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol. Microbiol. 51, 675-690. doi: 10.1046/j.1365-2958.2003.03877.x.
13. Ghafoor, A., Hay, I.D., and Rehm, B.H. (2011). Role of exopolysaccharides in Pseudomonas aeruginosa biofilm formation and architecture. Appl. Environ. Microbiol. 77, 5238-5246. doi: 10.1128/AEM. 00637-11.
14. Hentzer, M., Eberl, L., and Givskov, M. (2005). Transcriptome analysis of Pseudomonas aeruginosa biofilm development: anaerobic respiration and iron limitation. Biofilms 2, 37-61. doi: 10.1017/S1479050505001699.
15. Hentzer, M., Teitzel, G.M., Balzer, G.J., Heydorn, A., Molin, S., Givskov, M., et al. (2001). Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J. Bacteriol. 183, 5395-5401. doi: 10.1128/JB.183.18.5395-5401.2001.
16. Jackson, K.D., Starkey, M., Kremer, S., Parsek, M.R., and Wozniak, D.J. (2004). Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J. Bacteriol. 186, 4466-4475. doi: 10.1128/jb.186.14.4466-4475.2004.
17. Korber, D., Lawrence, J., Hendry, M., and Caldwell, D. (1993). Analysis of spatial variability within Mot+ and Mot- Pseudomonas fluorescens biofilms using representative elements. Biofouling 7, 339-358. doi: 10.1080/08927019309386264.
18. Lambertsen, L., Sternberg, C., and Molin, S. (2004). Mini-Tn7 transposons for site-specific tagging of bacteria with fluorescent proteins. Environ. Microbiol. 6, 726-732. doi: 10.1111/j.1462-2920.2004.00605.x.
19. Lee, K.W., Arumugam, K., Purbojati, R.W., Tay, Q.X., Williams, R.B., Kjelleberg, S., et al. (2013). Draft genome sequence of Klebsiella pneumoniae strain KP-1. Gen. Announc. 1:e01082-13. doi: 10.1128/genomeA. 01082-13.
20. Lee, K.W., Periasamy, S., Mukherjee, M., Xie, C., Kjelleberg, S., and Rice, S.A. (2014). Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. ISME J. 8, 894-907. doi: 10.1038/ismej.2013.194.
21. Lim, Y.W., Schmieder, R., Haynes, M., Willner, D., Furlan, M., Youle, M., et al. (2013). Metagenomics and metatranscriptomics: windows on CF-associated viral and microbial communities. J. Cyst. Fibros. 12, 154-164. doi: 10.1016/j.jcf.2012.07.009.
22. Ma, L., Conover, M., Lu, H., Parsek, M.R., Bayles, K., and Wozniak, D.J. (2009). Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog. 5:e1000354. doi: 10.1371/journal.ppat.1000354.
23. Ma, L., Jackson, K.D., Landry, R.M., Parsek, M.R., and Wozniak, D.J. (2006). Analysis of Pseudomonas aeruginosa conditional psl variants reveals roles for the psl polysaccharide in adhesion and maintaining biofilm structure postattachment. J. Bacteriol. 188, 8213-8221. doi: 10.1128/jb.01202-06.
24. Mathee, K., Ciofu, O., Sternberg, C., Lindum, P.W., Campbell, J.I., Jensen, P., et al. (1999). Mucoid conversion of Pseudomonas aeruginosa by hydrogen peroxide: a mechanism for virulence activation in the cystic fibrosis lung. Microbiology 145, 1349-1357. doi: 10.1099/13500872-145-6-1349.
25. Matsukawa, M., and Greenberg, E.P. (2004). Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development. J. Bacteriol. 186, 4449-4456. doi: 10.1128/jb.186.14.4449-4456.2004.
26. Miller, V.L., and Mekalanos, J.J. (1988). A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170, 2575-2583.
27. Ophir, T., and Gutnick, D.L. (1994). A role for exopolysaccharides in the protection of microorganisms from desiccation. Appl. Environ. Microbiol. 60, 740-745.
28. O'Toole, G.A. (2003). To build a biofilm. J. Bacteriol. 185, 2687-2689. doi: 10.1128/JB.185.9.2687-2689.2003.
29. Parsek, M.R., and Singh, P.K. (2003). Bacterial biofilms: an emerging link to disease pathogenesis. Annu. Rev. Microbiol. 57, 677-701. doi: 10.1146/annurev.micro.57.030502.090720.
30. Pier, G.B., Coleman, F., Grout, M., Franklin, M., and Ohman, D.E. (2001). Role of alginate O acetylation in resistance of mucoid Pseudomonas aeruginosa to opsonic phagocytosis. Infect. Immun. 69, 1895-1901. doi: 10.1128/iai.69.3.1895-1901.2001.
31. Ramette, A., Frapolli, M., Fischer-Le Saux, M., Gruffaz, C., Meyer, J.M., Defago, G., et al. (2011). Pseudomonas protegens sp. nov., widespread plant-protecting bacteria producing the biocontrol compounds 2,4-diacetylphloroglucinol and pyoluteorin. Syst. Appl. Microbiol. 34, 180-188. doi: 10.1016/j.syapm.2010.10.005.
32. Ryder, C., Byrd, M., and Wozniak, D.J. (2007). Role of polysaccharides in Pseudomonas aeruginosa biofilm development. Curr. Opin. Microbiol. 10, 644-648. doi: 10.1016/j.mib.2007.09.010.
33. Sternberg, C., and Tolker-Nielsen, T. (2006). Growing and analyzing biofilms in flow cells. Curr. Protoc. Microbiol. 00:B:1B.2:1B.2.1-1B.2.15. doi: 10.1002/9780471729259.mc01b02s00.
34. Stoodley, P., Sauer, K., Davies, D.G., and Costerton, J.W. (2002). Biofilms as complex differentiated communities. Ann. Rev. Microbiol. 56, 187-209. doi: 10.1146/annurev.micro.56.012302.160705.
35. Waite, R.D., Papakonstantinopoulou, A., Littler, E., and Curtis, M.A. (2005). Transcriptome analysis of Pseudomonas aeruginosa growth: comparison of gene expression in planktonic cultures and developing and mature biofilms. J. Bacteriol. 187, 6571-6576. doi: 10.1128/JB.187.18.6571-6576.2005.
36. Whiteley, M., Bangera, M.G., Bumgarner, R.E., Parsek, M.R., Teitzel, G.M., Lory, S., et al. (2001). Gene expression in Pseudomonas aeruginosa biofilms. Nature 413, 860-864. doi: 10.1038/35101627.
37. Wolfaardt, G., Lawrence, J., Robarts, R., Caldwell, S., and Caldwell, D. (1994). Multicellular organization in a degradative biofilm community. Appl. Environ. Microbiol. 60, 434-446.
38. Yanisch-Perron, C., Vieira, J., and Messing, J. (1985). Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33, 103-119. doi: 10.1016/0378-1119(85)90120-9.
39. Zhao, K., Tseng, B.S., Beckerman, B., Jin, F., Gibiansky, M.L., Harrison, J.J., et al. (2013). Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms. Nature 497, 388-391. doi: 10.1038/nature12155.