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Open Access 01-12-2014 | Research

Variations in motility and biofilm formation of Salmonella enterica serovar Typhi

Authors: Kalaivani Kalai Chelvam, Lay Ching Chai, Kwai Lin Thong

Published in: Gut Pathogens | Issue 1/2014

Abstract

Background

Salmonella enterica serovar Typhi (S. Typhi) exhibits unique characteristics as an intracellular human pathogen. It causes both acute and chronic infection with various disease manifestations in the human host only. The principal factors underlying the unique lifestyle of motility and biofilm forming ability of S. Typhi remain largely unknown. The main objective of this study was to explore and investigate the motility and biofilm forming behaviour among S. Typhi strains of diverse background.

Results

Swim and swarm motility tests were performed with 0.25% and 0.5% agar concentration, respectively; while biofilm formation was determined by growing the bacterial cultures for 48 hrs in 96-well microtitre plate. While all S. Typhi strains demonstrated swarming motility with smooth featureless morphology, 58 out of 60 strains demonstrated swimming motility with featureless or bull’s eye morphology. Interestingly, S. Typhi strains of blood-borne origin exhibited significantly higher swimming motility (P < 0.05) than stool-borne strains suggesting that swimming motility may play a role in the systemic invasion of S. Typhi in the human host. Also, stool-borne S. Typhi displayed a negative relationship between motility and biofilm forming behaviour, which was not observed in the blood-borne strains.

Conclusion

In summary, both swimming and swarming motility are conserved among S. Typhi strains but there was variation for biofilm forming ability. There was no difference observed in this phenotype for S. Typhi strains from diverse background. These findings serve as caveats for future studies to understand the lifestyle and transmission of this pathogen.

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Ramsey MM, Whiteley M: Pseudomonas aeruginosa attachment and biofilm development in dynamic environments. Mol Microbiol. 2004, 53 (4): 1075-1087. 10.1111/j.1365-2958.2004.04181.x.PubMed

Chellappa ST, Maredia R, Phipps K, Haskins WE, Weitao T: Motility of Pseudomonas aeruginosa contributes to SOS-inducible biofilm formation. Res Microbiol. 2013, 164 (10): 1019-1027. 10.1016/j.resmic.2013.10.001.PubMed

Houry A, Briandet R, Aymerich S, Gohar M: Involvement of motility and flagella in Bacillus cereus biofilm formation. Microbiology. 2009, 156 (4): 1009-1018.PubMed

Fraser GM, Hughes C: Swarming motility. Curr Opin Microbiol. 1999, 2 (6): 630-635. 10.1016/S1369-5274(99)00033-8.PubMed

Harshey RM, Matsuyama T: Dimorphic transition in Escherichia coli and Salmonella Typhimurium: surface-induced differentiation into hyperflagellate swarmer cells. Proc Natl Acad Sci USA. 1994, 91 (18): 8631-8635. 10.1073/pnas.91.18.8631.PubMedCentralPubMed

Kearns DB: A field guide to bacterial swarming motility. Nat Rev Microbiol. 2010, 8 (9): 634-644. 10.1038/nrmicro2405.PubMedCentralPubMed

Murray TS, Ledizet M, Kazmierczak BI: Swarming motility, secretion of type 3 effectors and biofilm formation phenotypes exhibited within a large cohort of Pseudomonas aeruginosa clinical isolates. J Med Microbiol. 2010, 59 (5): 511-520. 10.1099/jmm.0.017715-0.PubMedCentralPubMed

Branda SS, Vik S, Friedman L, Kolter R: Biofilms: the matrix revisited. Trends Microbiol. 2005, 13 (1): 20-26. 10.1016/j.tim.2004.11.006.PubMed

Hall-Stoodley L, Stoodley P: Evolving concepts in biofilm infections. Cell Microbiol. 2009, 11 (7): 1034-1043. 10.1111/j.1462-5822.2009.01323.x.PubMed

10.

Jensen PØ, Givskov M, Bjarnsholt T, Moser C: The immune system vs Pseudomonas aeruginosa biofilms. FEMS Immunol Med Mic. 2010, 59 (3): 292-305.

11.

Peters BM, Jabra-Rizk MA, Graeme A, Costerton JW, Shirtliff ME: Polymicrobial interactions: impact on pathogenesis and human disease. Clin Microbiol Rev. 2012, 25 (1): 193-213. 10.1128/CMR.00013-11.PubMedCentralPubMed

12.

Crawford RW, Rosales-Reyes R, Ramirez-Aguilar ML, Chapa-Azuela O, Alpuche-Aranda C, Gunn JS: Gallstones play a significant role in Salmonella spp. gallbladder colonization and carriage. Proc Natl Acad Sci USA. 2010, 107 (9): 4353-4358. 10.1073/pnas.1000862107.PubMedCentralPubMed

13.

Crump JA, Mintz ED: Global trends in typhoid and paratyphoid fever. Clin Infect Dis. 2010, 50 (2): 241-246. 10.1086/649541.PubMedCentralPubMed

14.

Black RE, Cisneros L, Levine MM, Banfi A, Lobos H, Rodriguez H: Case-control study to identify risk factors for paediatric endemic typhoid fever in Santiago, Chile. Bull World Health Organ. 1985, 63 (5): 899-904.PubMedCentralPubMed

15.

Gasem MH, Dolmans W, Keuter M, Djokomoeljanto R: Poor food hygiene and housing as risk factors for typhoid fever in Semarang, Indonesia. Trop Med Int Health. 2001, 6 (6): 484-490. 10.1046/j.1365-3156.2001.00734.x.PubMed

16.

Vollard Albert M, Ali S, van Asten AGH H, Widjaja S, Visser Leo G, Surjadi C, van Dissel Jaap T: Risk factors for typhoid and paratyphoid fever in Jakarta, Indonesia. J Am Med Assoc. 2004, 291 (21): 2607-2615. 10.1001/jama.291.21.2607.

17.

Lewis MD, Serichantalergs O, Pitarangsi C, Chuanak N, Mason CJ, Regmi LR, Pandey P, Laskar R, Shrestha CD, Malla S: Typhoid fever a massive, single–point source, multidrug-resistant outbreak in Nepal. Clin Infect Dis. 2005, 40: 554-610. 10.1086/427503.PubMed

18.

Crawford RW, Reeve KE, Gunn JS: Flagellated but not hyperfimbriated Salmonella enterica serovar Typhimurium attaches to and forms biofilms on cholesterol-coated surfaces. J Bacteriology. 2010, 192 (12): 2981-2990. 10.1128/JB.01620-09.

19.

Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM: Microbial biofilms. Annu Rev Microbiol. 1995, 49 (1): 711-745. 10.1146/annurev.mi.49.100195.003431.PubMed

20.

Shirtliff ME, Mader JT, Camper AK: Molecular interactions in biofilms. Chem Biol. 2002, 9 (8): 859-871. 10.1016/S1074-5521(02)00198-9.PubMed

21.

Liu SL, Ezaki T, Miura H, Matsui K, Yabuuchi E: Intact motility as a Salmonella Typhi invasion-related factor. Infect Immun. 1988, 56 (8): 1967-1973.PubMedCentralPubMed

22.

Kim W, Surette MG: Prevalence of surface swarming behavior in Salmonella. J Bacteriology. 2005, 187 (18): 6580-6583. 10.1128/JB.187.18.6580-6583.2005.

23.

Darnton NC, Turner L, Rojevsky S, Berg HC: Dynamics of bacterial swarming. Biophys J. 2010, 98 (10): 2082-2090. 10.1016/j.bpj.2010.01.053.PubMedCentralPubMed

24.

Kearns DB, Losick R: Swarming motility in undomesticated Bacillus subtilis. Mol Microbiol. 2003, 49 (3): 581-590.PubMed

25.

Armbruster CE, Mobley HL: Merging mythology and morphology: the multifaceted lifestyle of Proteus mirabilis. Nat Rev Microbiol. 2012, 10 (11): 743-754. 10.1038/nrmicro2890.PubMedCentralPubMed

26.

Belas R, Schneider R, Melch M: Characterization of Proteus mirabilis precocious swarming mutants: identification of rsbA, encoding a regulator of swarming behavior. J Bacteriology. 1998, 180 (23): 6126-6139.

27.

Chai LC, Kong BH, Elemfareji OI, Thong KL: Variable carbon catabolism among Salmonella enterica serovar Typhi isolates. PLoS ONE. 2012, 7 (5): e36201-10.1371/journal.pone.0036201.PubMedCentralPubMed

28.

Salcedo SP, Noursadeghi M, Cohen J, Holden DW: Intracellular replication of Salmonella Typhimurium strains in specific subsets of splenic macrophages in vivo. Cell Microbiol. 2001, 3 (9): 587-597. 10.1046/j.1462-5822.2001.00137.x.PubMed

29.

Sheppard M, Webb C, Heath F, Mallows V, Emilianus R, Maskell D, Mastroeni P: Dynamics of bacterial growth and distribution within the liver during Salmonella infection. Cell Microbiol. 2003, 5 (9): 593-600. 10.1046/j.1462-5822.2003.00296.x.PubMed

30.

Gibson D, White A, Snyder S, Martin S, Heiss C, Azadi P, Surette M, Kay W: Salmonella produces an O-antigen capsule regulated by AgfD and important for environmental persistence. J Bacteriology. 2006, 188 (22): 7722-7730. 10.1128/JB.00809-06.

31.

Jonas K, Tomenius H, Kader A, Normark S, Römling U, Belova L, Melefors Ö: Roles of curli, cellulose and BapA in Salmonella biofilm morphology studied by atomic force microscopy. BMC Microbiol. 2007, 7 (1): 70-10.1186/1471-2180-7-70.PubMedCentralPubMed

32.

Ledeboer NA, Jones BD: Exopolysaccharide sugars contribute to biofilm formation by Salmonella enterica serovar Typhimurium on HEp-2 cells and chicken intestinal epithelium. J Bacteriology. 2005, 187 (9): 3214-3226. 10.1128/JB.187.9.3214-3226.2005.

33.

Romling U, Rohde M, Olsen A, Normark S, Reinkoster J: AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella Typhimurium regulates at least two independent pathways. Mol Microbiol. 2000, 36 (1): 10-23. 10.1046/j.1365-2958.2000.01822.x.PubMed

34.

Römling U: Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol Life Sci CMLS. 2005, 62 (11): 1234-1246. 10.1007/s00018-005-4557-x.PubMed

35.

White AP, Surette MG: Comparative genetics of the rdar morphotype in Salmonella. J Bacteriology. 2006, 188 (24): 8395-8406. 10.1128/JB.00798-06.

36.

Romling U, Bokranz W, Rabsch W, Zogaj X, Nimtz M, Tschape H: Occurrence and regulation of the multicellular morphotype in Salmonella serovars important in human disease. Int J Med Microbiol. 2003, 293 (4): 273-285. 10.1078/1438-4221-00268.PubMed

37.

Pratt LA, Kolter R: Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol. 1998, 30 (2): 285-293. 10.1046/j.1365-2958.1998.01061.x.PubMed

38.

Vestby LK, Møretrø T, Ballance S, Langsrud S, Nesse LL: Survival potential of wild type cellulose deficient Salmonella from the feed industry. BMC Vet Res. 2009, 5 (1): 43-10.1186/1746-6148-5-43.PubMedCentralPubMed

39.

Solano C, García B, Valle J, Berasain C, Ghigo JM, Gamazo C, Lasa I: Genetic analysis of Salmonella Enteritidis biofilm formation: critical role of cellulose. Mol Microbiol. 2002, 43 (3): 793-808. 10.1046/j.1365-2958.2002.02802.x.PubMed

40.

White AP, Gibson DL, Collinson SK, Banser PA, Kay WW: Extracellular polysaccharides associated with thin aggregative fimbriae of Salmonella enterica serovar Enteritidis. J Bacteriology. 2003, 185 (18): 5398-5407. 10.1128/JB.185.18.5398-5407.2003.

41.

Verstraeten N, Braeken K, Debkumari B, Fauvart M, Fransaer J, Vermant J, Michiels J: Living on a surface: swarming and biofilm formation. Trends Microbiol. 2008, 16 (10): 496-506. 10.1016/j.tim.2008.07.004.PubMed

42.

O'Toole GA, Kolter R: Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol. 1998, 30 (2): 295-304. 10.1046/j.1365-2958.1998.01062.x.PubMed

43.

Simm R, Morr M, Kader A, Nimtz M, Römling U: GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol. 2004, 53 (4): 1123-1134. 10.1111/j.1365-2958.2004.04206.x.PubMed

44.

Römling U, Amikam D: Cyclic di-GMP as a second messenger. Curr Opin Microbiol. 2006, 9 (2): 218-228. 10.1016/j.mib.2006.02.010.PubMed

45.

Pratt JT, McDonough E, Camilli A: PhoB regulates motility, biofilms, and cyclic di-GMP in Vibrio cholerae. J Bacteriology. 2009, 191 (21): 6632-6642. 10.1128/JB.00708-09.

46.

Pehl MJ, Jamieson WD, Kong K, Forbester JL, Fredendall RJ, Gregory GA, McFarland JE, Healy JM, Orwin PM: Genes that influence swarming motility and biofilm formation in Variovorax paradoxus EPS. PloS ONE. 2012, 7 (2): e31832-10.1371/journal.pone.0031832.PubMedCentralPubMed

47.

Morrison RB, Scott A: Swarming of Proteus - a solution to an old problem. Nature. 1966, 211 (5046): 255-257. 10.1038/211255a0.PubMed

48.

Belas R, Simon M, Silverman M: Regulation of lateral flagella gene transcription in Vibrio. J Bacteriology. 1986, 167 (1): 210-218.

49.

Vazquez-Torres A, Jones-Carson J, Bäumler AJ, Falkow S, Valdivia R, Brown W, Le M, Berggren R, Parks WT, Fang FC: Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature. 1999, 401 (6755): 804-808. 10.1038/44593.PubMed

50.

Richter-Dahlfors A, Buchan AMJ, Finlay BB: Murine salmonellosis studied by confocal microscopy: Salmonella Typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J Exp Med. 1997, 186 (4): 569-580. 10.1084/jem.186.4.569.PubMedCentralPubMed

51.

Muñoz-Elías EJ, McKinney JD: Carbon metabolism of intracellular bacteria. Cell Microbiol. 2006, 8 (1): 10-22. 10.1111/j.1462-5822.2005.00648.x.PubMed

52.

Monack DM, Mueller A, Falkow S: Persistent bacterial infections: the interface of the pathogen and the host immune system. Nat Rev Microbiol. 2004, 2 (9): 747-765. 10.1038/nrmicro955.PubMed

53.

Harrison JJ, Wade WD, Akierman S, Vacchi-Suzzi C, Stremick CA, Turner RJ, Ceri H: The chromosomal toxin gene yafQ is a determinant of multidrug tolerance for Escherichia coli growing in a biofilm. Antimicrob Agents Chemother. 2009, 53 (6): 2253-2258. 10.1128/AAC.00043-09.PubMedCentralPubMed

54.

Thong KL, Cheong YM, Puthucheary S, Koh CL, Pang T: Epidemiologic Analysis of Sporadic Salmonella Typhi Isolates and Those from Outbreaks by Pulsed-Field Gel Electrophoresis. J Clin Microbiol. 1994, 32 (5): 1135-1141.PubMedCentralPubMed

55.

Thong KL, Cordano A-M, Rohani MY, Pang T: Molecular analysis of environmental and human isolates of Salmonella Typhi. Appl Environ Microbiol. 1996, 62 (1): 271-274.PubMedCentralPubMed

56.

Thong KL, Passey M, Clegg A, Combs GB, Rohani MY, Pang T: Molecular analysis of isolates of Salmonella Typhi obtained from patients with fatal and non-fatal typhoid fever. J Clin Microbiol. 1996, 34 (4): 1029-1033.PubMedCentralPubMed

57.

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 (3): 449-461. 10.1046/j.1365-2958.1998.00797.x.PubMed

58.

Stepanovic S, Cirkovic I, Ranin L, Svabic-Vlahovic M: Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Lett Appl Microbiol. 2004, 38 (5): 428-432. 10.1111/j.1472-765X.2004.01513.x.PubMed

59.

Ceri H, Olson ME, Stremick C, Read RR, Morck D, Buret A: The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol. 1999, 37 (6): 1771-1776.PubMedCentralPubMed

60.

Harrison JJ, Stremick CA, Turner RJ, Allan ND, Olson ME, Ceri H: Microtiter susceptibility testing of microbes growing on peg lids: a miniaturized biofilm model for high-throughput screening. Nat Protoc. 2010, 5 (7): 1236-1254. 10.1038/nprot.2010.71.PubMed

Title: Variations in motility and biofilm formation of Salmonella enterica serovar Typhi
Authors: Kalaivani Kalai Chelvam
Lay Ching Chai
Kwai Lin Thong
Publication date: 01-12-2014
Publisher: BioMed Central
Published in: Gut Pathogens / Issue 1/2014
Electronic ISSN: 1757-4749
DOI: https://doi.org/10.1186/1757-4749-6-2

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Variations in motility and biofilm formation of Salmonella enterica serovar Typhi

Abstract

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Results

Conclusion

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