Evidence for coexistence of distinct escherichia coli populations in various aquatic environments and their survival in estuary water

Applied and Environmental Microbiology

Volumn 79, Issue 15, 2013, Pages 4684-4693

  Berthe, T ^a   Ratajczak M , ^a   Clermont O , ^b   Denamur, E ^b   Petit, F ^a  

^a UNIVERSITÉ DE ROUEN   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AQUATIC ENVIRONMENTS; BACTERIAL INDICATORS; FECAL CONTAMINATION; INTESTINAL ENTEROCOCCI; MICROBIOLOGICAL QUALITY; MICROCOSM EXPERIMENTS; PHYSICOCHEMICAL CHARACTERISTICS; WATER ENVIRONMENTS;

ESCHERICHIA COLI; WATER QUALITY;

WATER POLLUTION;

ANTIINFECTIVE AGENT; ESCHERICHIA COLI PROTEIN; VIRULENCE FACTOR;

ANTIBIOTICS; BIOINDICATOR; COEXISTENCE; COLIFORM BACTERIUM; COMMENSAL; ESTUARINE ENVIRONMENT; MICROCOSM; PHYSICOCHEMICAL PROPERTY; SURVIVAL; VIRULENCE; WATER QUALITY;

ANTIBIOTIC RESISTANCE; ARTICLE; BIOFILM; CLASSIFICATION; DICTYOSTELIUM; ESCHERICHIA COLI; ESTUARY; FECES; FOOD CHAIN; FRANCE; GENETICS; GENOTYPE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; RIVER; WATER POLLUTION;

ANTI-BACTERIAL AGENTS; BIOFILMS; DICTYOSTELIUM; DRUG RESISTANCE, MICROBIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; ESTUARIES; FECES; FOOD CHAIN; FRANCE; GENOTYPE; POLYMERASE CHAIN REACTION; RIVERS; VIRULENCE FACTORS; WATER POLLUTION;

EID: 84880669396     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00698-13     Document Type: Article

References (49)

1. Croxen MA, Finlay BB. 2010. Molecular mechanisms of Escherichia coli pathogenicity. Nat. Rev. Microbiol. 8:26-38.
2. Kaper JB, Nataro JP, Mobley HL. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2:123-140.
3. Tenaillon O, Skurnik D, Picard B, Denamur E. 2010. The population genetics of commensal Escherichia coli. Nat. Rev. Microbiol. 8:207-217.
4. Clermont O, Bonacorsi S, Bingen E. 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 66:4555-4558.
5. Gordon DM, Clermont O, Tolley H, Denamur E. 2008. Assigning Escherichia coli strains to phylogenetic groups: multilocus sequence typing versus the PCR triplex method. Environ. Microbiol. 10:2484-2496.
6. Walk ST, Alm EW, Gordon DM, Ram JL, Toranzos GA, Tiedje JM, Whittam TS. 2009. Cryptic lineages of the genus Escherichia. Appl. Environ. Microbiol. 75:6534-6544.
7. Clermont O, Gordon DM, Brisse S, Walk ST, Denamur E. 2011. Characterization of the cryptic Escherichia lineages: rapid identification and prevalence. Environ. Microbiol. 13:2468-2477.
8. Luo C, Walk ST, Gordon DM, Feldgarden M, Tiedje JM, Konstantinidis KT. 2011. Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species. Proc. Natl. Acad. Sci. U. S. A. 108:7200-7205.
9. Ingle DJ, Clermont O, Skurnik D, Denamur E, Walk ST, Gordon DM. 2011. Biofilm formation by and thermal niche and virulence characteristics of Escherichia spp. Appl. Environ. Microbiol. 77:2695-2700.
10. Duriez P, Clermont O, Bonacorsi S, Bingen E, Chaventre A, Elion J, Picard B, Denamur E. 2001. Commensal Escherichia coli isolates are phylogenetically distributed among geographically distinct human populations. Microbiology 147:1671-1676.
11. Gordon DM, Cowling A. 2003. The distribution and genetic structure of Escherichia coli in Australian vertebrates: host and geographic effects. Microbiology 149:3575-3586.
12. Skurnik D, Bonnet D, Bernède-Bauduin C, Michel R, Guette C, Becker JM, Balaire C, Chau F, Mohler J, Jarlier V, Boutin JP, Moreau B, Guillemot D, Denamur E, Andremont A, Ruimy R. 2008. Characteristics of human intestinal Escherichia coli with changing environments. Environ. Microbiol. 10:2132-2137.
13. Ratajczak M, Laroche E, Berthe T, Clermont O, Pawlak B, Denamur E, Petit F. 2010. Influence of hydrological conditions on the Escherichia coli population structure in the water of a creek on a rural watershed. BMC Microbiol. 10:222.
14. Walk ST, Alm EW, Calhoun LM, Mladonicky JM, Whittam TS. 2007. Genetic diversity and population structure of Escherichia coli isolated from freshwater beaches. Environ. Microbiol. 9:2274-2288.
15. Ishii S, Ksoll WB, Hicks RE, Sadowsky MJ. 2006. Presence and growth of naturalized Escherichia coli in temperate soils from Lake Superior watersheds. Appl. Environ. Microbiol. 72:612-621.
16. Brennan FP, O'Flaherty V, Kramers G, Grant J, Richards KG. 2010. Long-term persistence and leaching of Escherichia coli in temperate maritime soils. Appl. Environ. Microbiol. 76:1449-1455.
17. Lyautey E, Lu Z, Lapen DR, Wilkes G, Scott A, Berkers T, Edge TA, Topp E. 2010. Distribution and diversity of Escherichia coli populations in the South Nation River drainage basin, eastern Ontario, Canada. Appl. Environ. Microbiol. 76:1486-1496.
18. Van Elsas JD, Semenov AV, Costa R, Trevors JT. 2010. Survival of Escherichia coli in the environment: fundamental and public health aspects. ISME J. 5:173-183.
19. Rozen Y, Belkin S. 2001. Survival of enteric bacteria in seawater. FEMS Microbiol. Rev. 25:513-529.
20. Pachepsky YA, Shelton DR. 2011. Escherichia coli and fecal coliforms in freshwater and estuarine sediments. Crit. Rev. Environ. Sci. Technol. 41: 1067-1110.
21. Garcia-Armisen T, Servais P. 2009. Partitioning and fate of particleassociated E. coli in river waters. Water Environ. Res. 81:21-28.
22. Moreira S, Brown A, Ha R, IserhoffK, Yim M, Yang J, Liao B, Pszczolko E, Qin W, Leung KT. 2012. Persistence of Escherichia coli in freshwater periphyton: biofilm-forming capacity as a selective advantage. FEMS Microbiol. Ecol. 79:608-618.
23. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, Bidet P, Bingen E, Bonacorsi S, Bouchier C, Bouvet O, Calteau A, Chiapello H, Clermont O, Cruveiller S, Danchin A, Diard M, Dossat C, Karoui ME, Frapy E, Garry L, Ghigo JM, Gilles AM, Johnson J, Le Bouguenec C, Lescat M, Mangenot S, Martinez-Jehanne V, Matic I, Nassif X, Oztas S, Petit MA, Pichon C, Rouy Z, Ruf CS, Schneider D, Tourret J, Vacherie B, Vallenet D, Medigue C, Rocha EP, Denamur E. 2009. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet. 5:e1000344. doi:10.1371/journal.pgen.1000344.
24. Sabarly V, Bouvet O, Glodt J, Clermont O, Skurnik D, Diancourt L, De Vienne D, Denamur E, Dillmann C. 2011. The decoupling between genetic structure and metabolic phenotypes in Escherichia coli leads to continuous phenotypic diversity. J. Evol. Biol. 24:1559-1571.
25. Goto DK, Yan T. 2011. Genotypic diversity of Escherichia coli in the water and soil of tropical watersheds in Hawaii. Appl. Environ. Microbiol. 77: 3988-3997.
26. Power ML, Littlefield-Wyer J, Gordon DM, Veal DA, Slade MB. 2005. Phenotypic and genotypic characterization of encapsulated Escherichia coli isolated from blooms in two Australian lakes. Environ. Microbiol. 7:631-640.
27. Guerrini M-C, Mouchel JM, Meybeck M, Penven MJ, Hubert G, Muxart T. 1998. Le bassin de la Seine: la confrontation du rural et de l'urbain, p 29-75. In Meybeck M, de Marsily G, Fustec É (ed), La Seine en son basin: fonctionnement ècologique d'un système fluvial anthropisè, la fiche dètaillèe du livre. Elsevier, Paris, France.
28. Servais P, Garcia-Armisen T, George I, Billen G. 2007. Fecal bacteria in the rivers of the Seine drainage network (France): sources, fate and modelling. Sci. Total Environ. 375:152-167.
29. Touron A, Berthe T, Gargala G, Fournier M, Ratajczak M, Servais P, Petit F. 2007. Assessment of fecal contamination and the relationship between pathogens and fecal bacterial indicators in an estuarine environment (Seine, France). Mar. Pollut. Bull. 54:1441-1450.
30. Oberlè K, Capdeville MJ, Berthe T, Budzinski H, Petit F. 2012. Evidence for a complex relationship between antibiotics and antibiotic-resistant Escherichia coli: from medical center patients to a receiving environment. Environ. Sci. Technol. 46:1859-1868.
31. Moissenet D, Salauze B, Clermont O, Bingen E, Arlet G, Denamur E, Merens A, Mitanchez D, Vu-Thien H. 2010. Meningitis caused by Escherichia coli producing TEM-52 extended-spectrum beta-lactamase within an extensive outbreak in a neonatal ward: epidemiological investigation and characterization of the strain. J. Clin. Microbiol. 48:2459-2463.
32. Lescat M, Clermont O, Woerther PL, Glodt J, Dion S, Skurnik D, Djossou F, Dupont C, Perroz G, Picard B. 2013. Commensal Escherichia coli strains in Guiana reveal a high genetic diversity with host-dependent population structure. Environ. Microbiol. Rep. 5:49-57.
33. Clermont O, Olier M, Hoede C, Diancourt L, Brisse S, Keroudean M, Glodt J, Picard B, Oswald E, Denamur E. 2011. Animal and human pathogenic Escherichia coli strains share common genetic backgrounds. Infect. Genet. Evol. 11:654-662.
34. Clermont O, Johnson JR, Menard M, Denamur E. 2007. Determination of Escherichia coli O types by allele-specific polymerase chain reaction: application to the O types involved in human septicemia. Diagn. Microbiol. Infect. Dis. 57:129-136.
35. Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M. 2000. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J. Microbiol. Methods 40:175-179.
36. Comitè de l'Antibiogramme de la Sociètè Franèaise de Microbiologie. 2001. Communiquè du comitè de l'antibiogramme de la sociètè franèaise de microbiologie, p 2-13. Sociètè Franèaise de Microbiologie, Paris, France.
37. Adiba S, Nizak C, Van Baalen M, Denamur E, Depaulis F. 2010. From grazing resistance to pathogenesis: the coincidental evolution of virulence factors. PLoS One 5:e11882. doi:10.1371/journal.pone.0011882.
38. Membrè JM, Leporq B, Vialette M, Mettler E, Perrier L, Thuault D, Zwietering M. 2005. Temperature effect on bacterial growth rate: quantitative microbiology approach including cardinal values and variability estimates to perform growth simulations on/in food. Int. J. Food Microbiol. 100:179-186.
39. Dick LK, Stelzer EA, Bertke EE, Fong DL, Stoeckel DM. 2010. Relative decay of Bacteroidales microbial source tracking markers and cultivated Escherichia coli in freshwater microcosms. Appl. Environ. Microbiol. 76: 3255-3262.
40. Gordon DM, Bauer S, Johnson JR. 2002. The genetic structure of Escherichia coli populations in primary and secondary habitats. Microbiology 148:1513-1522.
41. Bergholz PW, Noar JD, Buckley DH. 2011. Environmental patterns are imposed on the population structure of Escherichia coli after fecal deposition. Appl. Environ. Microbiol. 77:211-219.
42. Byappanahalli MN, Whitman RL, Shively DA, Sadowsky MJ, Ishii S. 2006. Population structure, persistence, and seasonality of autochthonous Escherichia coli in temperate, coastal forest soil from a Great Lakes watershed. Environ. Microbiol. 8:504-513.
43. Mèric G, Kemsley EK, Falush D, Saggers EJ, Lucchini S. 2013. Phylogenetic distribution of traits associated with plant colonization in Escherichia coli. Environ. Microbiol. 15:487-501.
44. Masters N, Wiegand A, Ahmed W, Katouli M. 2011. Escherichia coli virulence genes profile of surface waters as an indicator of water quality. Water Res. 45:6321-6333.
45. Janezic KJ, Ferry B, Hendricks EW, Janiga BA, Johnson T, Murphy S, Roberts ME, Scott SM, Theisen AN, Hung KF, Daniel SL. 2013. Phenotypic and genotypic characterization of Escherichia coli isolated from untreated surface waters. Open Microbiol. J. 7:9-19.
46. Vignaroli C, Luna G, Rinaldi C, Di Cesare A, Danovaro R, Biavasco F. 2012. New sequence types and multidrug resistance among pathogenic Escherichia coli isolates from coastal marine sediments. Appl. Environ. Microbiol. 78:3916-3922.
47. Muirhead RW, Collins RP, Bremer PJ. 2006. Interaction of Escherichia coli and soil particles in runoff. Appl. Environ. Microbiol. 72:3406-3411.
48. Berthe T, Touron A, Leloup J, Deloffre J, Petit F. 2008. Fecal-indicator bacteria and sedimentary processes in estuarine mudflats (Seine, France). Mar. Pollut. Bull. 57:59-67.
49. Droppo IG, Liss SN, Williams D, Nelson T, Jaskot C, Trapp B. 2009. Dynamic existence of waterborne pathogens within river sediment compartments. Implications for water quality regulatory affairs. Environ. Sci. Technol. 43:1737-1743.