Enhanced biofilm formation and multi-host transmission evolve from divergent genetic backgrounds in Campylobacter jejuni

Environmental Microbiology

Volumn 17, Issue 11, 2015, Pages 4779-4789

  Pascoe, Ben ^a   Méric, Guillaume ^a   Murray, Susan ^a   Yahara, Koji ^a,b,e   Mageiros, Leonardos ^a   Bowen, Ryan ^a   Jones, Nathan H ^a   Jeeves, Rose E ^a,f   Lappin Scott, Hilary M ^a   Asakura, Hiroshi ^c   Sheppard, Samuel K ^a,d  

^a SWANSEA UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF TOKYO   (Japan)

^c NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e KURUME UNIVERSITY   (Japan)

^f PUBLIC HEALTH ENGLAND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

OXYGEN;

BIOFILM; CAMPYLOBACTER JEJUNI; CLASSIFICATION; EVOLUTION; GENETIC BACKGROUND; GENETIC VARIATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; GROWTH, DEVELOPMENT AND AGING; HUMAN; ISOLATION AND PURIFICATION; METABOLISM;

BIOFILMS; BIOLOGICAL EVOLUTION; CAMPYLOBACTER JEJUNI; GENETIC BACKGROUND; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; HUMANS; OXYGEN;

EID: 84949239443     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.13051     Document Type: Article

References (72)

1. Alam, M.T., Petit, R.A., 3rd, Crispell, E.K., Thornton, T.A., Conneely, K.N., Jiang, Y., etal. (2014) Dissecting vancomycin-intermediate resistance in Staphylococcus aureus using genome-wide association. Genome Biol Evol 6: 1174-1185.
2. van Alphen, L.B., Wenzel, C.Q., Richards, M.R., Fodor, C., Ashmus, R.A., Stahl, M., etal. (2014) Biological roles of the O-methyl phosphoramidate capsule modification in Campylobacter jejuni. PLoS ONE 9: e87051.
3. Asakura, H., Yamasaki, M., Yamamoto, S., and Igimi, S. (2007) Deletion of peb4 gene impairs cell adhesion and biofilm formation in Campylobacter jejuni. FEMS Microbiol Lett 275: 278-285.
4. Asakura, H., Bruggemann, H., Sheppard, S.K., Ekawa, T., Meyer, T.F., Yamamoto, S., and Igimi, S. (2012) Molecular evidence for the thriving of Campylobacter jejuni ST-4526 in Japan. PLoS ONE 7: e48394.
5. van Asselt, E.D., Jacobs-Reitsma, W.F., van Brakel, R., van der Voet, H., and van der Fels-Klerx, H.J. (2008) Campylobacter prevalence in the broiler supply chain in the Netherlands. Poult Sci 87: 2166-2172.
6. Avila-Ramirez, C., Tinajero-Trejo, M., Davidge, K.S., Monk, C.E., Kelly, D.J., and Poole, R.K. (2013) Do globins in microaerophilic Campylobacter jejuni confer nitrosative stress tolerance under oxygen limitation? Antioxid Redox Signal 18: 424-431.
7. Barnard, F.M., Loughlin, M.F., Fainberg, H.P., Messenger, M.P., Ussery, D.W., Williams, P., and Jenks, P.J. (2004) Global regulation of virulence and the stress response by CsrA in the highly adapted human gastric pathogen Helicobacter pylori. Mol Microbiol 51: 15-32.
8. Bobrov, A.G., Kirillina, O., and Perry, R.D. (2007) Regulation of biofilm formation in Yersinia pestis. Adv Exp Med Biol 603: 201-210.
9. Brooks, J.L., and Jefferson, K.K. (2014) Phase variation of poly-N-acetylglucosamine expression in Staphylococcus aureus. PLoS Pathog 10: e1004292.
10. Bull, S.A., Allen, V.M., Domingue, G., Jorgensen, F., Frost, J.A., Ure, R., etal. (2006) Sources of Campylobacter spp. colonizing housed broiler flocks during rearing. Appl Environ Microbiol 72: 645-652.
11. Cabello, H., Torres, A., Celis, R., El-Ebiary, M., Puig de la Bellacasa, J., Xaubet, A., etal. (1997) Bacterial colonization of distal airways in healthy subjects and chronic lung disease: a bronchoscopic study. Eur Respir J 10: 1137-1144.
12. Carver, T., Thomson, N., Bleasby, A., Berriman, M., and Parkhill, J. (2009) DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 25: 119-120.
13. Christner, M., Franke, G.C., Schommer, N.N., Wendt, U., Wegert, K., Pehle, P., etal. (2010) The giant extracellular matrix-binding protein of Staphylococcus epidermidis mediates biofilm accumulation and attachment to fibronectin. Mol Microbiol 75: 187-207.
14. Christner, M., Heinze, C., Busch, M., Franke, G., Hentschke, M., Bayard Duhring, S., etal. (2012) sarA negatively regulates Staphylococcus epidermidis biofilm formation by modulating expression of 1 MDa extracellular matrix binding protein and autolysis-dependent release of eDNA. Mol Microbiol 86: 394-410.
15. Coffey, B.M., and Anderson, G.G. (2014) Biofilm formation in the 96-well microtiter plate. Methods Mol Biol 1149: 631-641.
16. Craddock, N., Hurles, M.E., Cardin, N., Pearson, R.D., Plagnol, V., Robson, S., etal. (2010) Genome-wide association study of CNVs in 16, 000 cases of eight common diseases and 3, 000 shared controls. Nature 464: 713-720.
17. Didelot, X., and Falush, D. (2007) Inference of bacterial microevolution using multilocus sequence data. Genetics 175: 1251-1266.
18. Dingle, K.E., Colles, F.M., Wareing, D.R., Ure, R., Fox, A.J., Bolton, F.E., etal. (2001) Multilocus sequence typing system for Campylobacter jejuni. J Clin Microbiol 39: 14-23.
19. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
20. Falush, D., and Bowden, R. (2006) Genome-wide association mapping in bacteria? Trends Microbiol 14: 353-355.
21. Fields, J.A., and Thompson, S.A. (2008) Campylobacter jejuni CsrA mediates oxidative stress responses, biofilm formation, and host cell invasion. J Bacteriol 190: 3411-3416.
22. Fouts, D.E., Mongodin, E.F., Mandrell, R.E., Miller, W.G., Rasko, D.A., Ravel, J., etal. (2005) Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PLoS Biol 3: e15.
23. Frirdich, E., Biboy, J., Adams, C., Lee, J., Ellermeier, J., Gielda, L.D., etal. (2012) Peptidoglycan-modifying enzyme Pgp1 is required for helical cell shape and pathogenicity traits in Campylobacter jejuni. PLoS Pathog 8: e1002602.
24. 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.
25. Golz, G., Sharbati, S., Backert, S., and Alter, T. (2012) Quorum sensing dependent phenotypes and their molecular mechanisms in Campylobacterales. Eur J Microbiol Immunol (Bp) 2: 50-60.
26. Guerry, P. (2007) Campylobacter flagella: not just for motility. Trends Microbiol 15: 456-461.
27. Guerry, P., Ewing, C.P., Schirm, M., Lorenzo, M., Kelly, J., Pattarini, D., etal. (2006) Changes in flagellin glycosylation affect Campylobacter autoagglutination and virulence. Mol Microbiol 60: 299-311.
28. Gundogdu, O., Bentley, S.D., Holden, M.T., Parkhill, J., Dorrell, N., and Wren, B.W. (2007) Re-annotation and re-analysis of the Campylobacter jejuni NCTC11168 genome sequence. BMC Genomics 8: 162.
29. Gundogdu, O., Mills, D.C., Elmi, A., Martin, M.J., Wren, B.W., and Dorrell, N. (2011) The Campylobacter jejuni transcriptional regulator Cj1556 plays a role in the oxidative and aerobic stress response and is important for bacterial survival in vivo. J Bacteriol 193: 4238-4249.
30. Hendrixson, D.R., Akerley, B.J., and DiRita, V.J. (2001) Transposon mutagenesis of Campylobacter jejuni identifies a bipartite energy taxis system required for motility. Mol Microbiol 40: 214-224.
31. Howlett, R.M., Hughes, B.M., Hitchcock, A., and Kelly, D.J. (2012) Hydrogenase activity in the foodborne pathogen Campylobacter jejuni depends upon a novel ABC-type nickel transporter (NikZYXWV) and is SlyD-independent. Microbiology 158: 1645-1655.
32. Jolley, K.A., and Maiden, M.C. (2010) BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11: 595.
33. Joshua, G.W., Guthrie-Irons, C., Karlyshev, A.V., and Wren, B.W. (2006) Biofilm formation in Campylobacter jejuni. Microbiology 152: 387-396.
34. Kalmokoff, M., Lanthier, P., Tremblay, T.L., Foss, M., Lau, P.C., Sanders, G., etal. (2006) Proteomic analysis of Campylobacter jejuni 11168 biofilms reveals a role for the motility complex in biofilm formation. J Bacteriol 188: 4312-4320.
35. Laabei, M., Recker, M., Rudkin, J.K., Aldeljawi, M., Gulay, Z., Sloan, T.J., etal. (2014) Predicting the virulence of MRSA from its genome sequence. Genome Res doi: 10.1101/gr.165415.113.
36. 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.
37. Liu, X., Sun, X., Wu, Y., Xie, C., Zhang, W., Wang, D., etal. (2013) Oxidation-sensing regulator AbfR regulates oxidative stress responses, bacterial aggregation, and biofilm formation in Staphylococcus epidermidis. J Biol Chem 288: 3739-3752.
38. McElroy, K.E., Hui, J.G., Woo, J.K., Luk, A.W., Webb, J.S., Kjelleberg, S., etal. (2014) Strain-specific parallel evolution drives short-term diversification during Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci USA 111: E1419-E1427.
39. Mack, D., Nedelmann, M., Krokotsch, A., Schwarzkopf, A., Heesemann, J., and Laufs, R. (1994) Characterization of transposon mutants of biofilm-producing Staphylococcus epidermidis impaired in the accumulative phase of biofilm production: genetic identification of a hexosamine-containing polysaccharide intercellular adhesin. Infect Immun 62: 3244-3253.
40. Malde, A., Gangaiah, D., Chandrashekhar, K., Pina-Mimbela, R., Torrelles, J.B., and Rajashekara, G. (2014) Functional characterization of exopolyphosphatase/guanosine pentaphosphate phosphohydrolase (PPX/GPPA) of Campylobacter jejuni. Virulence 5: 521-533.
41. Meric, G., Yahara, K., Mageiros, L., Pascoe, B., Maiden, M.C., Jolley, K.A., and Sheppard, S.K. (2014) A reference pan-genome approach to comparative bacterial genomics: identification of novel epidemiological markers in pathogenic Campylobacter. PLoS ONE 9: e92798.
42. Oh, E., and Jeon, B. (2014) Role of alkyl hydroperoxide reductase (AhpC) in the biofilm formation of Campylobacter jejuni. PLoS ONE 9: e87312.
43. Otto, M. (2014) Physical stress and bacterial colonization. FEMS Microbiol Rev 38 (6): 1250-1270.
44. Parkhill, J., Wren, B.W., Mungall, K., Ketley, J.M., Churcher, C., Basham, D., etal. (2000) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403: 665-668.
45. Parkhill, J., Dougan, G., James, K.D., Thomson, N.R., Pickard, D., Wain, J., etal. (2001) Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413: 848-852.
46. Pearson, A.D., Greenwood, M., Healing, T.D., Rollins, D., Shahamat, M., Donaldson, J., and Colwell, R.R. (1993) Colonization of broiler chickens by waterborne Campylobacter jejuni. Appl Environ Microbiol 59: 987-996.
47. Pearson, B.M., Gaskin, D.J., Segers, R.P., Wells, J.M., Nuijten, P.J., and van Vliet, A.H. (2007) The complete genome sequence of Campylobacter jejuni strain 81116 (NCTC11828). J Bacteriol 189: 8402-8403.
48. Price, M.N., Dehal, P.S., and Arkin, A.P. (2010) FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5: e9490.
49. Revez, J., Rossi, M., Ellstrom, P., de Haan, C., Rautelin, H., and Hanninen, M.L. (2011) Finnish Campylobacter jejuni strains of multilocus sequence type ST-22 complex have two lineages with different characteristics. PLoS ONE 6: e26880.
50. Rohde, H., Burandt, E.C., Siemssen, N., Frommelt, L., Burdelski, C., Wurster, S., etal. (2007) Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections. Biomaterials 28: 1711-1720.
51. Rohde, H., Frankenberger, S., Zahringer, U., and Mack, D. (2010) Structure, function and contribution of polysaccharide intercellular adhesin (PIA) to Staphylococcus epidermidis biofilm formation and pathogenesis of biomaterial-associated infections. Eur J Cell Biol 89: 103-111.
52. Sheppard, S.K., McCarthy, N.D., Falush, D., and Maiden, M.C. (2008) Convergence of Campylobacter species: implications for bacterial evolution. Science 320: 237-239.
53. Sheppard, S.K., Dallas, J.F., Strachan, N.J., MacRae, M., McCarthy, N.D., Wilson, D.J., etal. (2009) Campylobacter genotyping to determine the source of human infection. Clin Infect Dis 48: 1072-1078.
54. Sheppard, S.K., Dallas, J.F., Wilson, D.J., Strachan, N.J., McCarthy, N.D., Jolley, K.A., etal. (2010) Evolution of an agriculture-associated disease causing Campylobacter coli clade: evidence from national surveillance data in Scotland. PLoS ONE 5: e15708.
55. Sheppard, S.K., Colles, F.M., McCarthy, N.D., Strachan, N.J., Ogden, I.D., Forbes, K.J., etal. (2011) Niche segregation and genetic structure of Campylobacter jejuni populations from wild and agricultural host species. Mol Ecol 20: 3484-3490.
56. Sheppard, S.K., Jolley, K.A., and Maiden, M.C. (2012) A gene-by-gene approach to bacterial population genomics: whole genome MLST of Campylobacter. Genes (Basel) 3: 261-277.
57. Sheppard, S.K., Didelot, X., Meric, G., Torralbo, A., Jolley, K.A., Kelly, D.J., etal. (2013a) Genome-wide association study identifies vitamin B5 biosynthesis as a host specificity factor in Campylobacter. Proc Natl Acad Sci USA 110: 11923-11927.
58. Sheppard, S.K., Didelot, X., Jolley, K.A., Darling, A.E., Pascoe, B., Meric, G., etal. (2013b) Progressive genome-wide introgression in agricultural Campylobacter coli. Mol Ecol 22: 1051-1064.
59. Sheppard, S.K., Cheng, L., Meric, G., De Haan, C.P.A., Llarena, A.-K., Marttinen, P., etal. (2014) Cryptic ecology among host generalist Campylobacter jejuni in domestic animals. Mol Ecol 23: 2442-2451.
60. Solano, C., Echeverz, M., and Lasa, I. (2014) Biofilm dispersion and quorum sensing. Curr Opin Microbiol 18: 96-104.
61. Spiliopoulou, A.I., Krevvata, M.I., Kolonitsiou, F., Harris, L.G., Wilkinson, T.S., Davies, A.P., etal. (2012) An extracellular Staphylococcus epidermidis polysaccharide: relation to Polysaccharide Intercellular Adhesin and its implication in phagocytosis. BMC Microbiol 12: 76.
62. Sulaeman, S., Hernould, M., Schaumann, A., Coquet, L., Bolla, J.M., De, E., and Tresse, O. (2012) Enhanced adhesion of Campylobacter jejuni to abiotic surfaces is mediated by membrane proteins in oxygen-enriched conditions. PLoS ONE 7: e46402.
63. Svensson, S.L., Davis, L.M., MacKichan, J.K., Allan, B.J., Pajaniappan, M., Thompson, S.A., and Gaynor, E.C. (2009) The CprS sensor kinase of the zoonotic pathogen Campylobacter jejuni influences biofilm formation and is required for optimal chick colonization. Mol Microbiol 71: 253-272.
64. Svensson, S.L., Pryjma, M., and Gaynor, E.C. (2014) Flagella-mediated adhesion and extracellular DNA release contribute to biofilm formation and stress tolerance of Campylobacter jejuni. PLoS ONE 9: e106063.
65. Taboada, B., Ciria, R., Martinez-Guerrero, C.E., and Merino, E. (2012) ProOpDB: Prokaryotic Operon DataBase. Nucleic Acids Res 40: D627-D631.
66. Trachoo, N., and Frank, J.F. (2002) Effectiveness of chemical sanitizers against Campylobacter jejuni-containing biofilms. J Food Prot 65: 1117-1121.
67. Valle, J., Latasa, C., Gil, C., Toledo-Arana, A., Solano, C., Penades, J.R., and Lasa, I. (2012) Bap, a biofilm matrix protein of Staphylococcus aureus prevents cellular internalization through binding to GP96 host receptor. PLoS Pathog 8: e1002843.
68. Wellcome Trust Case Control Consortium (2007) Genome-wide association study of 14, 000 cases of seven common diseases and 3, 000 shared controls. Nature 447: 661-678.
69. Woolhouse, M.E., Taylor, L.H., and Haydon, D.T. (2001) Population biology of multihost pathogens. Science 292: 1109-1112.
70. Woolhouse, M.E., Haydon, D.T., and Antia, R. (2005) Emerging pathogens: the epidemiology and evolution of species jumps. Trends Ecol Evol 20: 238-244.
71. Wu, Y., Zhu, T., Han, H., Liu, H., Xu, T., Francois, P., etal. (2014) Staphylococcus epidermidis SrrAB regulates bacterial growth and biofilm formation differently under oxic and micro-aerobic conditions. J Bacteriol 197 (3): 459-476.
72. Zimmer, M., Barnhart, H., Idris, U., and Lee, M.D. (2003) Detection of Campylobacter jejuni strains in the water lines of a commercial broiler house and their relationship to the strains that colonized the chickens. Avian Dis 47: 101-107.