Pseudomonas aeruginosa-derived rhamnolipids and other detergents modulate colony morphotype and motility in the Burkholderia cepacia complex

Journal of Bacteriology

Volumn 199, Issue 13, 2017, Pages

  Bernier, Steve P ^a   Hum, Courtney ^a   Li, Xiang ^b   O'Toole, George A ^c   Magarvey, Nathan A ^b   Surette, Michael G ^a,b  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Burkholderia; Polymicrobial interactions; Pseudomonas aeruginosa; Rhamnolipids; Swarming motility

Indexed keywords

BACTERIAL TOXIN; DETERGENT; RHAMNOLIPID; CULTURE MEDIUM; GLYCOLIPID;

ARTICLE; BACTERIAL VIRULENCE; BACTERIUM COLONY; BURKHOLDERIA CEPACIA COMPLEX; CODING; GENE; IN VITRO STUDY; MICROORGANISM; MORPHOTYPE; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; TRANSPOSON; ANTIBIOTIC RESISTANCE; CULTURE MEDIUM; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; MOVEMENT (PHYSIOLOGY); PHYSIOLOGY;

BURKHOLDERIA CEPACIA COMPLEX; CULTURE MEDIA; DETERGENTS; DRUG RESISTANCE, BACTERIAL; GLYCOLIPIDS; MOVEMENT; MUTAGENESIS, INSERTIONAL; PSEUDOMONAS AERUGINOSA;

EID: 85020713028     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00171-17     Document Type: Article

References (59)

1. Duan K, Sibley CD, Davidson CJ, Surette MG. 2009. Chemical interactions between organisms in microbial communities. Contrib Microbiol 16: 1-17. https://doi.org/10.1159/000219369
2. Keller L, Surette MG. 2006. Communication in bacteria: an ecological and evolutionary perspective. Nat Rev Microbiol 4:249-258. https://doi.org/10.1038/nrmicro1383
3. Lyon GJ, Muir TW. 2003. Chemical signaling among bacteria and its inhibition. Chem Biol 10:1007-1021. https://doi.org/10.1016/j.chembiol .2003.11.003
4. Rath CM, Dorrestein PC. 2012. The bacterial chemical repertoire mediates metabolic exchange within gut microbiomes. Curr Opin Microbiol 15:147-154. https://doi.org/10.1016/j.mib.2011.12.009
5. Cornforth DM, Foster KR. 2013. Competition sensing: the social side of bacterial stress responses. Nat Rev Microbiol 11:285-293. https://doi.org/10.1038/nrmicro2977
6. Foster KR, Bell T. 2012. Competition, not cooperation, dominates interactions among culturable microbial species. Curr Biol 22:1845-1850. https://doi.org/10.1016/j.cub.2012.08.005
7. Bernier SP, Surette MG. 2013. Concentration-dependent activity of antibiotics in natural environments. Front Microbiol 4:20. https://doi.org/10 .3389/fmicb.2013.00020
8. Davies J, Ryan KS. 2012. Introducing the parvome: bioactive compounds in the microbial world. ACS Chem Biol 7:252-259. https://doi.org/10 .1021/cb200337h
9. Davies J, Spiegelman GB, Yim G. 2006. The world of subinhibitory antibiotic concentrations. Curr Opin Microbiol 9:445-453. https://doi .org/10.1016/j.mib.2006.08.006
10. Hoffman LR, D'Argenio DA, MacCoss MJ, Zhang Z, Jones RA, Miller SI. 2005. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436:1171-1175. https://doi.org/10.1038/nature03912
11. Yim G, Wang HH, Davies J. 2007. Antibiotics as signalling molecules. Philos Trans R Soc Lond B Biol Sci 362:1195-1200. https://doi.org/10 .1098/rstb.2007.2044
12. Carmody LA, Zhao J, Kalikin LM, LeBar W, Simon RH, Venkataraman A, Schmidt TM, Abdo Z, Schloss PD, LiPuma JJ. 2015. The daily dynamics of cystic fibrosis airway microbiota during clinical stability and at exacerbation. Microbiome 3:12. https://doi.org/10.1186/s40168-015-0074-9
13. Harrison F. 2007. Microbial ecology of the cystic fibrosis lung. Microbiology 153:917-923. https://doi.org/10.1099/mic.0.2006/004077-0
14. Schwab U, Abdullah LH, Perlmutt OS, Albert D, Davis CW, Arnold RR, Yankaskas JR, Gilligan P, Neubauer H, Randell SH, Boucher RC. 2014. Localization of Burkholderia cepacia complex bacteria in cystic fibrosis lungs and interactions with Pseudomonas aeruginosa in hypoxic mucus. Infect Immun 82:4729-4745. https://doi.org/10.1128/IAI.01876-14
15. Bernier SP, Workentine ML, Li X, Magarvey NA, O'Toole GA, Surette MG. 2016. Cyanide toxicity to Burkholderia cenocepacia is modulated by polymicrobial communities and environmental factor. Front Microbiol 7:725
16. Smalley NE, An D, Parsek MR, Chandler JR, Dandekar AA. 2015. Quorum sensing protects Pseudomonas aeruginosa against cheating by other species in a laboratory coculture model. J Bacteriol 197:3154-3159. https://doi.org/10.1128/JB.00482-15
17. Burrows LL. 2012. Pseudomonas aeruginosa twitching motility: type IV pili in action. Annu Rev Microbiol 66:493-520. https://doi.org/10.1146/annurev-micro-092611-150055
18. Bjarnsholt T, Jensen PO, Jakobsen TH, Phipps R, Nielsen AK, Rybtke MT, Tolker-Nielsen T, Givskov M, Hoiby N, Ciofu O, Scandinavian Cystic Fibrosis Study Consortium. 2010. Quorum sensing and virulence of Pseudomonas aeruginosa during lung infection of cystic fibrosis patients. PLoS One 5:e10115. https://doi.org/10.1371/journal.pone.0010115
19. LiPuma JJ. 2010. The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev 23:299-323. https://doi.org/10.1128/CMR.00068-09
20. Caiazza NC, Shanks RM, O'Toole GA. 2005. Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacteriol 187: 7351-7361. https://doi.org/10.1128/JB.187.21.7351-7361.2005
21. Déziel E, Lepine F, Milot S, Villemur R. 2003. rhlA is required for the production of a novel biosurfactant promoting swarming motility in Pseudomonas aeruginosa: 3-(3-hydroxyalkanoyloxy)alkanoic acids (HAAs), the precursors of rhamnolipids. Microbiology 149:2005-2013. https://doi.org/10.1099/mic.0.26154-0
22. Tremblay J, Richardson AP, Lepine F, Deziel E. 2007. Self-produced extracellular stimuli modulate the Pseudomonas aeruginosa swarming motility behaviour. Environ Microbiol 9:2622-2630. https://doi.org/10 .1111/j.1462-2920.2007.01396.x
23. Bernier SP, Nguyen DT, Sokol PA. 2008. A LysR-type transcriptional regulator in Burkholderia cenocepacia influences colony morphology and virulence. Infect Immun 76:38-47. https://doi.org/10.1128/IAI.00874-07
24. Bernier SP, Sokol PA. 2005. Use of suppression-subtractive hybridization to identify genes in the Burkholderia cepacia complex that are unique to Burkholderia cenocepacia. J Bacteriol 187:5278-5291. https://doi.org/10 .1128/JB.187.15.5278-5291.2005
25. Lewenza S, Visser MB, Sokol PA. 2002. Interspecies communication between Burkholderia cepacia and Pseudomonas aeruginosa. Can J Microbiol 48:707-716. https://doi.org/10.1139/w02-068
26. Huber B, Riedel K, Hentzer M, Heydorn A, Gotschlich A, Givskov M, Molin S, Eberl L. 2001. The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 147:2517-2528. https://doi.org/10.1099/00221287-147-9-2517
27. Shaligram NS, Singhal RS. 2010. Surfactin-a review on biosynthesis, fermentation, purification and applications. Food Technol Biotechnol 48:119-134
28. Nandkumar MA, Ashna U, Thomas LV, Nair PD. 2015. Pulmonary surfactant expression analysis-role of cell-cell interactions and 3-D tissue-like architecture. Cell Biol Int 39:272-282. https://doi.org/10 .1002/cbin.10389
29. Bernier SP, Letoffe S, Delepierre M, Ghigo JM. 2011. Biogenic ammonia modifies antibiotic resistance at a distance in physically separated bacteria. Mol Microbiol 81:705-716. https://doi.org/10.1111/j.1365-2958 .2011.07724.x
30. Das P, Yang XP, Ma LZ. 2014. Analysis of biosurfactants from industrially viable Pseudomonas strain isolated from crude oil suggests how rhamnolipids congeners affect emulsification property and antimicrobial activity. Front Microbiol 5:696
31. Lee HH, Molla MN, Cantor CR, Collins JJ. 2010. Bacterial charity work leads to population-wide resistance. Nature 467:82-85. https://doi.org/10.1038/nature09354
32. Létoffe S, Audrain B, Bernier SP, Delepierre M, Ghigo JM. 2014. Aerial exposure to the bacterial volatile compound trimethylamine modifies antibiotic resistance of physically separated bacteria by raising culture medium pH. mBio 5(1):e00944-13. https://doi.org/10.1128/mBio .00944-13
33. Shatalin K, Shatalina E, Mironov A, Nudler E. 2011. H2S: a universal defense against antibiotics in bacteria. Science 334:986-990. https://doi .org/10.1126/science.1209855
34. Vega NM, Allison KR, Khalil AS, Collins JJ. 2012. Signaling-mediated bacterial persister formation. Nat Chem Biol 8:431-433. https://doi.org/10.1038/nchembio.915
35. de Bentzmann S, Aurouze M, Ball G, Filloux A. 2006. FppA, a novel Pseudomonas aeruginosa prepilin peptidase involved in assembly of type IVb pili. J Bacteriol 188:4851-4860. https://doi.org/10.1128/JB .00345-06
36. Kachlany SC, Planet PJ, DeSalle R, Fine DH, Figurski DH. 2001. Genes for tight adherence of Actinobacillus actinomycetemcomitans: from plaque to plague to pond scum. Trends Microbiol 9:429-437. https://doi.org/10.1016/S0966-842X(01)02161-8
37. Tomich M, Planet PJ, Figurski DH. 2007. The tad locus: postcards from the widespread colonization island. Nat Rev Microbiol 5:363-375. https://doi.org/10.1038/nrmicro1636
38. 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. https://doi.org/10.1016/j.chom.2015.07.006
39. Mowat E, Paterson S, Fothergill JL, Wright EA, Ledson MJ, Walshaw MJ, Brockhurst MA, Winstanley C. 2011. Pseudomonas aeruginosa population diversity and turnover in cystic fibrosis chronic infections. Am J Respir Crit Care Med 183:1674-1679. https://doi.org/10.1164/rccm.201009-1430OC
40. Winstanley C, O'Brien S, Brockhurst MA. 2016. Pseudomonas aeruginosa evolutionary adaptation and diversification in cystic fibrosis chronic lung infections. Trends Microbiol 24:327-337. https://doi.org/10.1016/j.tim .2016.01.008
41. 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. https://doi.org/10.1371/journal.pone.0060225
42. 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
43. Read RC, Roberts P, Munro N, Rutman A, Hastie A, Shryock T, Hall R, McDonald-Gibson W, Lund V, Taylor G, Cole PJ, Wilson R. 1992. Effect of Pseudomonas aeruginosa rhamnolipids on mucociliary transport and ciliary beating. J Appl Physiol 72:2271-2277
44. Kownatzki R, Tummler B, Doring G. 1987. Rhamnolipid of Pseudomonas aeruginosa in sputum of cystic fibrosis patients. Lancet i:1026-1027. https://doi.org/10.1016/S0140-6736(87)92286-0
45. Lieberman TD, Flett KB, Yelin I, Martin TR, McAdam AJ, Priebe GP, Kishony R. 2014. Genetic variation of a bacterial pathogen within individuals with cystic fibrosis provides a record of selective pressures. Nat Genet 46:82-87. https://doi.org/10.1038/ng.2848
46. Lieberman TD, Michel JB, Aingaran M, Potter-Bynoe G, Roux D, Davis MR, Jr, Skurnik D, Leiby N, LiPuma JJ, Goldberg JB, McAdam AJ, Priebe GP, Kishony R. 2011. Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat Genet 43:1275-1280. https://doi.org/10.1038/ng.997
47. Silva IN, Santos PM, Santos MR, Zlosnik JE, Speert DP, Buskirk SW, Bruger EL, Waters CM, Cooper VS, Moreira LM. 2016. Long-term evolution of Burkholderia multivorans during a chronic cystic fibrosis infection reveals shifting forces of selection. mSystems 1(3):e00029-16. https://doi.org/10 .1128/mSystems.00029-16
48. Al-Tahhan RA, Sandrin TR, Bodour AA, Maier RM. 2000. Rhamnolipidinduced removal of lipopolysaccharide from Pseudomonas aeruginosa: effect on cell surface properties and interaction with hydrophobic substrates. Appl Environ Microbiol 66:3262-3268. https://doi.org/10.1128/AEM.66.8.3262-3268.2000
49. Sotirova A, Spasova D, Vasileva-Tonkova E, Galabova D. 2009. Effects of rhamnolipid-biosurfactant on cell surface of Pseudomonas aeruginosa. Microbiol Res 164:297-303. https://doi.org/10.1016/j.micres.2007.01.005
50. Whang LM, Liu PW, Ma CC, Cheng SS. 2008. Application of biosurfactants, rhamnolipid, and surfactin, for enhanced biodegradation of dieselcontaminated water and soil. J Hazard Mater 151:155-163. https://doi .org/10.1016/j.jhazmat.2007.05.063
51. O'Grady EP, Sokol PA. 2011. Burkholderia cenocepacia differential gene expression during host-pathogen interactions and adaptation to the host environment. Front Cell Infect Microbiol 1:15
52. Bernard CS, Bordi C, Termine E, Filloux A, de Bentzmann S. 2009. Organization and PprB-dependent control of the Pseudomonas aeruginosa tad locus, involved in Flp pilus biology. J Bacteriol 191:1961-1973. https://doi.org/10.1128/JB.01330-08
53. Chung JW, Altman E, Beveridge TJ, Speert DP. 2003. Colonial morphology of Burkholderia cepacia complex genomovar III: implications in exopolysaccharide production, pilus expression, and persistence in the mouse. Infect Immun 71:904-909. https://doi.org/10.1128/IAI.71.2.904-909.2003
54. Hay ID, Wang Y, Moradali MF, Rehman ZU, Rehm BH. 2014. Genetics and regulation of bacterial alginate production. Environ Microbiol 16: 2997-3011. https://doi.org/10.1111/1462-2920.12389
55. 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. https://doi.org/10.1128/AEM.00682-06
56. Cardona ST, Mueller CL, Valvano MA. 2006. Identification of essential operons with a rhamnose-inducible promoter in Burkholderia cenocepacia. Appl Environ Microbiol 72:2547-2555. https://doi.org/10.1128/AEM .72.4.2547-2555.2006
57. Figurski DH, Helinski DR. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A 76:1648-1652. https://doi.org/10.1073/pnas.76.4.1648
58. Winsor GL, Khaira B, Van Rossum T, Lo R, Whiteside MD, Brinkman FS. 2008. The Burkholderia Genome Database: facilitating flexible queries and comparative analyses. Bioinformatics 24:2803-2804. https://doi.org/10.1093/bioinformatics/btn524
59. Workentine ML, Surette MG, Bernier SP. 2014. Draft genome sequence of Burkholderia dolosa PC543 isolated from cystic fibrosis airways. Genome Announc 2(1):e00043-14. https://doi.org/10.1128/genomeA.00043-14