Biofilm formation and detachment in gram-negative pathogens is modulated by select bile acids

PLoS ONE

Volumn 11, Issue 3, 2016, Pages

  Sanchez, Laura M ^a   Cheng, Andrew T ^a   Warner, Christopher J A ^a   Townsley, Loni ^a   Peach, Kelly C ^a   Navarro, Gabriel ^a   Shikuma, Nicholas J ^a   Bray, Walter M ^a   Riener, Romina M ^a   Yildiz, Fitnat H ^a   Linington, Roger G ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SIMON FRASER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BILE ACID; BILIRUBIN; CHENODEOXYCHOLIC AID; CHOLESTEROL; CHOLIC ACID; DEOXYCHOLIC ACID; FATTY ACID DERIVATIVE; GLYCOCHENODEOXYCHOLIC ACID; GLYCOCHOLIC ACID; GLYCODEOXYCHOLIC ACID; GLYCOLITHOCHOLIC ACID; LITHOCHOLIC ACID; PHOSPHORYLCHOLINE; TAUROCHENODEOXYCHOLIC ACID; TAUROCHOLIC ACID; TAURODEOXYCHOLIC ACID; TAUROLITHOCHOLIC ACID; UNCLASSIFIED DRUG;

ARTICLE; BIOFILM; BIOLOGICAL ACTIVITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; MEMBRANE FORMATION; NONHUMAN; PSEUDOMONAS AERUGINOSA; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; VALIDATION PROCESS; VIBRIO CHOLERAE; ANIMAL; FISH; GRAM NEGATIVE BACTERIUM; METABOLISM; PHYSIOLOGY; VALIDATION STUDY;

ANIMALS; BIOFILMS; FISHES; GRAM-NEGATIVE BACTERIA;

EID: 84962195199     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0149603     Document Type: Article

References (68)

1. Fong JCN, Syed KA, Klose KE, Yildiz FH. Role of Vibrio polysaccharide (vps) genes in VPS production, biofilm formation and Vibrio cholerae pathogenesis. Microbiology. 2010; 156(156):2757-69. doi: 10.1099/mic.0.040196-0
2. Franklin MJ, Nivens DE, Weadge JT, Howell PL. Biosynthesis of the Pseudomonas aeruginosa extracellular polysaccharides, alginate, Pel, and Psl. Front Microbiol. 2011; 2(2). doi: 10.3389/fmicb.2011.00167
3. Adal KA, Farr BM. Central venous catheter-related infections: A review. Nutrition. 1996; 12(12):208-13. doi: 10.1016/s0899-9007(96)91126-0 PMID: 8798227
4. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: A common cause of persistent infections. Science. 1999; 284(284):1318-22. doi: 10.1126/science.284.5418.1318 PMID: 10334980
5. Davies D. Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discovery. 2003; 2(2):114-22. doi: 10.1038/nrd1008 PMID: 12563302
6. Parsek MR, Singh PK. Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol. 2003; 57:677-701. doi: 10.1146/annurev.micro.57.030502.090720 PMID: 14527295
7. Bjarnsholt T, Ciofu O, Molin S, Givskov M, Hoiby N. Applying insights from biofilm biology to drug development - can a new approach be developed? Nat Rev Drug Discov. 2013; 12(12):791-808. doi: 10.1038/nrd4000 PMID: 24080700
8. Melander RJ, Melander C. Innovative strategies for combating biofilm-based infections. In: Donelli G, editor. Biofilm-based healthcare-associated infections. Advances in Experimental Medicine and Biology. 8312015. p. 69-91.
9. Rabin N, Zheng Y, Opoku-Temeng C, Du Y, Bonsu E, Sintim HO. Agents that inhibit bacterial biofilm formation. Future Med Chem. 2015; 7(7):647-71. doi: 10.4155/fmc.15.7 PMID: 25921403
10. Navarro G, Cheng AT, Peach KC, Bray WM, Bernan VS, Yildiz FH, et al. Image-based 384-well high-throughput screening method for the discovery of skyllamycins A to C as biofilm inhibitors and inducers of biofilm detachment in Pseudomonas aeruginosa. Antimicrob Agents Ch. 2014; 58(58):1092-9. doi: 10.1128/aac.01781-13
11. Peach KC, Bray WM, Shikuma NJ, Gassner NC, Lokey RS, Yildiz FH, et al. An image-based 384-well high-throughput screening method for the discovery of biofilm inhibitors in Vibrio cholerae. Mol Biosyst. 2011; 7(7):1176-84. doi: 10.1039/c0mb00276c PMID: 21246108
12. Sanchez LM, Wong WR, Riener RM, Schulze CJ, Linington RG. Examining the fish microbiome: vertebrate-derived bacteria as an environmental niche forthe discovery of unique marine natural products. PLoS One. 2012; 7(7):e35398. doi: 10.1371/journal.pone.0035398 PMID: 22574119
13. Hofmann AF, Eckmann L. How bile acids confer gut mucosal protection against bacteria. Proc Natl Acad Sci USA. 2006; 103(103):4333-4. doi: 10.1073/pnas.0600780103 PMID: 16537368
14. Hofmann AF. The enterohepatic circulation of bile acids in mammals: form and functions. Front Biosci. 2009; 14:2584-98.
15. Li T, Chiang JYL. Bile acid signaling in metabolic disease and drug therapy. Pharmacol Rev. 2014; 66(4):948-83. doi: 10.1124/pr.113.008201 PMID: 25073467
16. Crawford JM, Clardy J. Bacterial symbiontsand natural products. Chem Commun. 2011; 47(47):7559-66. doi: 10.1039/C1CC11574J
17. Donia MS, Fischbach MA. Small molecules from the human microbiota. Science. 2015; 349(349).
18. Noga EJ. Fish disease: diagnosis and treatment: John Wiley & Sons; 2010.
19. 1H NMR spectroscopy. Lipids. 2006; 41(41):591-603. doi: 10.1007/s11745-006-5008-7 PMID: 16981437
20. Kim SH, Yang HO, Sohn YC, Kwon HC. Aeromicrobiumhalocynthiaesp nov., a taurocholic acid-producing bacterium isolated from the marine ascidian Halocynthia roretzi. Int J Syst Evol Microbiol. 2010; 60:2793-8. doi: 10.1099/ijs.0.016618-0 PMID: 20081024
21. Kim D, Lee JS, Kim J, Kang SJ, Yoon JH, Kim WG, et al. Biosynthesis of bile acids in a variety of marine bacterial taxa. J Microbiol Biotechnol. 2007; 17(17):403-7. PMID: 18050942
22. Maneerat S, Nitoda T, Kanzaki H, Kawai F. Bile acids are new products of a marine bacterium, Myroides sp strain SM1. Appl Microbiol Biotechnol. 2005; 67(67):679-83. doi: 10.1007/s00253-004-1777-1 PMID: 15549287
23. Park SC, Kim CJ, Uramoto M, Yun HI, Yoon KH, Oh TK. Antibacterial substance produced by Streptococcus faecium under anaerobic culture. Biosci Biotechnol, Biochem. 1995; 59(59):1966-7.
24. Hagey LR, Moller PR, Hofmann AF, Krasowski MD. Diversity of bile salts in fish and amphibians: evolution of a complex biochemical pathway. Physiol Biochem Zool. 2010; 83(83):308-21. doi: 10.1086/649966 PMID: 20113173
25. Yang MH, Liu Z, Hughes C, Stern AM, Wang H, Zhong ZT, et al. Bile salt-induced intermolecular disulfide bond formation activates Vibrio cholerae virulence. Proc Natl Acad Sci USA. 2013; 110(110):2348-53. doi: 10.1073/pnas.1218039110 PMID: 23341592
26. Reen FJ, Woods DF, Mooij MJ, Adams C, O'Gara F. Respiratory pathogens adopt a chronic lifestyle in response to bile. Plos One. 2012; 7(7): e45978.doi: 10.1371/journal.pone.0045978 PMID: 23049911
27. Chen KM, Chiang MK, Wang ML, Ho HC, Lu MC, Lai YC. The role of pgaC in Klebsiella pneumoniae virulence and biofilm formation. Microb Pathog. 2014; 77:89-99. doi: 10.1016/j.micpath.2014.11.005 PMID: 25450884
28. Hennequin C, Forestier C. oxyR, a LysR-Type Regulator Involved in Klebsiella pneumoniae Mucosal and Abiotic Colonization. Infect Immun. 2009; 77(77):5449-57. doi: 10.1128/iai.00837-09 PMID: 19786563
29. Diard M, Garry L, Selva M, Mosser T, Denamur E, Matic I. Pathogenicity-associated islands in extraintestinal pathogenic Escherichia coli are fitness elements involved in intestinal colonization. J Bacteriol. 2010; 192(192):4885-93. doi: 10.1128/jb.00804-10 PMID: 20656906
30. Girard V, Cote JP, Charbonneau ME, Campos M, Berthiaume F, Hancock MA, et al. Conformation change in a self-recognizing autotransporter modulates bacterial cell-cell interaction. J Biol Chem. 2010; 285(285):10616-26. doi: 10.1074/jbc.M109.069070 PMID: 20123991
31. Sung JY, Shaffer EA, Lam K, Rususka I, Costerton JW. Hydrophobic bile-salt inhibits bacterial adhesion on biliary stent material Dig Dis Sci. 1994; 39(39):999-1006. doi: 10.1007/bf02087551 PMID: 8174442
32. Ante VM, Bina XR, Howard MF, Sayeed S, Bina JE. Vibrio cholerae leuO transcription is positively regulated by ToxR and contributes to bile resistance. J Bacteriol. 2015. doi: 10.1128/jb.00419-15
33. Hay AJ, Zhu J. Host intestinal signal-promoted biofilm dispersal induces Vibrio cholerae colonization. Infect Immun. 2015; 83(83):317-23. doi: 10.1128/iai.02617-14 PMID: 25368110
34. Hung DT, Zhu J, Sturtevant D, Mekalanos JJ. Bile acids stimulate biofilm formation in Vibrio cholerae. Mol Microbiol. 2006; 59(59):193-201. doi: 10.1111/j.1365-2958.2005.04846.x PMID: 16359328
35. Koestler BJ, Waters CM. Bile acids and bicarbonate inversely regulate intracellular cyclic di-GMP in Vibrio cholerae. Infect Immun. 2014; 82(82):3002-14. doi: 10.1128/iai.01664-14 PMID: 24799624
36. Koestler BJ, Waters CM. Intestinal GPS: bile and bicarbonate control cyclic di-GMP to provide Vibrio cholerae spatial cues within the small intestine. Gut Microbes. 2014; 5(5):775-80. doi: 10.4161/19490976.2014.985989 PMID: 25621620
37. Nesper J, Lauriano CM, Klose KE, Kapfhammer D, Kraiss A, Reidl J. Characterization of Vibrio cholerae O1 El Tor galU and galE mutants: Influence on lipopolysaccharide structure, colonization, and biofilm formation. Infect Immun. 2001; 69(69):435-45. doi: 10.1128/iai.69.1.435-445.2001 PMID: 11119535
38. Pagel M, Simonet V, Li J, Lallemand M, Lauman B, Delcour AH. Phenotypic characterization of pore mutants of the Vibrio cholerae porin Omp U. J Bacteriol. 2007; 189(189):8593-600. doi: 10.1128/jb.01163-07 PMID: 17905973
39. Chen C, Wang QB, Liu ZH, Zhao JJ, Jiang X, Sun HY, et al. Characterization of role of the toxR gene in the physiology and pathogenicity of Vibrio alginolyticus. Anton Leeuw Int J G. 2012; 101(101):281-8. doi: 10.1007/s10482-011-9632-8
40. Di Pietro A, Picerno I, Visalli G, Chirico C, Scoglio ME. Effects of "host factor" bile on adaptability and virulence of Vibrios, foodborne potential pathogenic agents. Annali di igiene: medicina preventiva e di comunita. 2004; 16(16):615-25.
41. Li X, Bossier P, Dierckens K, Laureau S, Defoirdt T. Impact of mucin, bile salts and cholesterol on the virulence of Vibrio anguillarum towards gnotobiotic sea bass (Dicentrarchus labrax) larvae. Vet Microbiol. 2015; 175(175):44-9. doi: 10.1016/j.vetmic.2014.10.033 PMID: 25465176
42. Li X, Defoirdt T, Bossier P. Relation between virulence of Vibrio anguillarum strains and response to the host factors mucin, bile salts and cholesterol. J Appl Microbiol. 2015; 119(119):25-32. doi: 10.1111/jam.12813 PMID: 25807847
43. Wang SY, Lauritz J, Jass J, Milton DL. Role for the major outer-membrane protein from Vibrio anguillarum in bile resistance and biofilm formation. Microbiology. 2003; 149:1061-71. doi: 10.1099/mic.0.26032-0 PMID: 12686648
44. Dale JL, Cagnazzo J, Phan CQ, Barnes AM, Dunny GM. Multiple roles for Enterococcus faecalis glycosyltransferases in biofilm-associated antibiotic resistance, cell envelope integrity, and conjugative transfer. Antimicrob Agents Ch. 2015; 59(59):4094-105. doi: 10.1128/aac.00344-15
45. Begley M, Kerr C, Hill C. Exposure to bile influences biofilm formation by Listeria monocytogenes. Gut Pathogens. 2009; 1(1):11. doi: 10.1186/1757-4749-1-11 PMID: 19476630
46. Ambalam P, Kondepudi KK, Nilsson I, Wadstrom T, Ljungh A. Bile enhances cell surface hydrophobicity and biofilm formation of Bifidobacteria. Appl Biochem Biotech. 2014; 172(172):1970-81. doi: 10.1007/s12010-013-0596-1
47. Amund OD, Ouoba LII, Sutherland JP, Ghoddusi HB. Assessing the effects of exposure to environmental stress on some functional properties of Bifidobacterium animalis ssp lactis. Benef Microbes. 2014; 5(4):461-9. doi: 10.3920/bm2013.0099 PMID: 25097108
48. Crawford RW, Gibson DL, Kay WW, Gunn JS. Identification of a bile-induced exopolysaccharide required for Salmonella biofilm formation on gallstone surfaces. Infect Immun. 2008; 76(76):5341-9. doi: 10.1128/iai.00786-08 PMID: 18794278
49. Lebeer S, Verhoeven TLA, Velez MP, Vanderleyden J, De Keersmaecker SCJ. Impact of environmental and genetic factors on biofilm formation by the probiotic strain Lactobacillus rhamnosus GG. Appl Environ Microbiol. 2007; 73(73):6768-75. doi: 10.1128/aem.01393-07 PMID: 17827316
50. Pumbwe L, Skilbeck CA, Nakano V, Avila-Campos MJ, Piazza RMF, Wexler HM. Bile salts enhance bacterial co-aggregation, bacterial-intestinal epithelial cell adhesion, biofilm formation and antimicrobial resistance of Bacteroides fragilis. Microb Pathogenesis. 2007; 43(2-3):78-87. doi: 10.1016/j.micpath.2007.04.002
51. Slizova M, Nemcova R, Mad'ar M, Hadryova J, Gancarcikova S, Popper M, et al. Analysis of biofilm formation by intestinal lactobacilli. Can J Microbiol. 2015; 61(61):437-46. doi: 10.1139/cjm-2015-0007 PMID: 25961850
52. Zaidi AH, Bakkes PJ, Krom BP, van der Mei HC, Driessen AJM. Cholate-stimulated biofilm formation by Lactococcuslactis Cells. Appl Environ Microbiol. 2011; 77(77):2602-10. doi: 10.1128/aem.01709-10 PMID: 21335382
53. Leung JW, Liu YL, Chan RCY, Ling TKW, Cheng AF. Effects of adherence factors and human bile on bacterial attachment and biliary stent blockage: an in vitro study. Gastrointest Endosc. 2002; 56(56):72-7. doi: 10.1067/mge.2002.125366 PMID: 12085038
54. Cerda-Maira FA, Ringelberg CS, Taylor RK. The bile response repressor BreR regulates expression of the Vibrio cholerae breAB efflux system operon. J Bacteriol. 2008; 190(190):7441-52. doi: 10.1128/jb.00584-08 PMID: 18776020
55. Almagro-Moreno S, Pruss K, Taylor RK. Intestinal colonization dynamics of Vibrio cholerae. PLoS Pathogens. 2015; 11(11):e1004787. doi: 10.1371/journal.ppat.1004787 PMID: 25996593
56. Chua SL, Liu Y, Yam JKH, Chen Y, Vejborg RM, Tan BGC, et al. Dispersed cells represent a distinct stage in the transition from bacterial biofilm to planktonic lifestyles. Nat Commun. 2014; 5(5). doi: 10.1038/ncomms5462
57. Inagaki T, Moschetta A, Lee YK, Peng L, Zhao GX, Downes M, et al. Regulation of antibacterial defense in the small intestine by the nuclear bile acid receptor. Proc Natl Acad Sci USA. 2006; 103(10):3920-5. doi: 10.1073/pnas.0509592103 PMID: 16473946
58. Xu Q, Dziejman M, Mekalanos JJ. Determination of the transcriptome of Vibrio cholerae during intraintestinal growth and midexponential phase in vitro. Proc Natl Acad Sci USA. 2003; 100(100):1286-91. doi: 10.1073/pnas.0337479100 PMID: 12552086
59. Bina JE, Mekalanos JJ. Vibrio cholerae tolC is required for bile resistance and colonization. Infect Immun. 2001; 69(69):4681-5. doi: 10.1128/iai.69.7.4681-4685.2001 PMID: 11402016
60. Bina JE, Provenzano D, Wang CM, Bina XWR, Mekalanos JJ. Characterization of the Vibrio cholerae vexAB and vexCD efflux systems. Arch Microbiol. 2006; 186(186):171-81. doi: 10.1007/s00203-006-0133-5 PMID: 16804679
61. Cerda-Maira FA, Kovacikova G, Jude BA, Skorupski K, Taylor RK. Characterization of BreR interaction with the bile response promoters breAB and breR in Vibrio cholerae. J Bacteriol. 2013; 195(195):307-17. doi: 10.1128/jb.02008-12 PMID: 23144245
62. Provenzano D, Klose KE. Altered expression of the ToxR-regulated porins OmpU and OmpT diminishes Vibrio cholerae bile resistance, virulence factor expression, and intestinal colonization. Proc Natl Acad Sci USA. 2000; 97(97):10220-4. doi: 10.1073/pnas.170219997 PMID: 10944196
63. Wibbenmeyer JA, Provenzano D, Landry CF, Klose KE, Delcour AH. Vibrio cholerae OmpU and OmpT porins are differentially affected by bile. Infect Immun. 2002; 70(70):121-6. PMID: 11748172
64. Devkota S, Wang YW, Musch MW, Leone V, Fehlner-Peach H, Nadimpalli A, et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10(-/-) mice. Nature. 2012; 487 (7405):104. doi: 10.1038/nature11225 PMID: 22722865
65. Kim TK, Garson MJ, Fuerst JA. Marine actinomycetes related to the 'Salinospora' group from the Great Barrier Reef sponge Pseudoceratina clavata. Environ Microbiol. 2005; 7(7):509-18. PMID: 15816928
66. Yildiz FH, Schoolnik GK. 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 USA. 1999; 96(96):4028-33. doi: 10.1073/pnas.96.7.4028 PMID: 10097157
67. Hickman JW, Tifrea DF, Harwood CS. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci USA. 2005; 102(102):14422-7. doi: 10.1073/pnas.0507170102 PMID: 16186483
68. O'Toole GA, Kolter R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol. 1998; 28(28):449-61. PMID: 9632250