Development of quantitative PCR assays targeting the 16s rRNA genes of enterococcus spp. and their application to the identification of enterococcus species in environmental samples

Applied and Environmental Microbiology

Volumn 79, Issue 1, 2013, Pages 196-204

  Ryu, Hodon ^a   Henson, Michael ^a   Elk, Michael ^a   Toledo Hernandez, Carlos ^a   Griffith, John ^b   Blackwood, Denene ^c   Noble, Rachel ^c   Gourmelon, Michèle ^d   Glassmeyer, Susan ^e   Santo Domingo, Jorge W ^a  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^b SOUTHERN CALIFORNIA COASTAL WATER RESEARCH PROJECT   (United States)

^c University of North Carolina at Chapel Hill   (United States)

^d IFREMER   (France)

^e U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA; 16S RRNA GENE; 16S RRNA GENE SEQUENCE; AMPLIFICATION RATE; ENTEROCOCCUS CASSELIFLAVUS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ENTEROCOCCUS SPP; ENVIRONMENTAL SAMPLE; ENVIRONMENTAL WATER SAMPLES; FECAL SAMPLES; NON-TARGETED; POSITIVE SIGNALS; QUANTITATIVE PCR; RELATIVE ABUNDANCE; WATER SAMPLES;

BACILLI; GENES; POLYMERASE CHAIN REACTION; RNA; SIGNAL DETECTION;

ASSAYS;

BACTERIAL DNA; BACTERIAL RNA; PRIMER DNA; RIBOSOME DNA; RNA 16S;

BACTERIUM; BIOASSAY; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; RELATIVE ABUNDANCE; SAMPLING; SPATIAL DISTRIBUTION; SPECIES DIVERSITY;

ARTICLE; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; ENTEROCOCCUS; EVALUATION; GENETIC VARIABILITY; GENETICS; ISOLATION AND PURIFICATION; METHODOLOGY; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; REAL TIME POLYMERASE CHAIN REACTION;

BACTERIOLOGICAL TECHNIQUES; DNA PRIMERS; DNA, BACTERIAL; DNA, RIBOSOMAL; ENTEROCOCCUS; ENVIRONMENTAL MICROBIOLOGY; GENETIC VARIATION; MOLECULAR SEQUENCE DATA; REAL-TIME POLYMERASE CHAIN REACTION; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

ENTEROCOCCUS; ENTEROCOCCUS CASSELIFLAVUS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM;

EID: 84871860476     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02802-12     Document Type: Article

References (43)

1. Muller T, Ulrich A, Ott EM, Muller M. 2001. Identification of plantassociated enterococci. J. Appl. Microbiol. 91:268-278.
2. Badgley BD, Nayak BS, Harwood VJ. 2010. The importance of sediment and submerged aquatic vegetation as potential habitats for persistent strains of enterococci in a subtropical watershed. Water Res. 44:5857-5866.
3. Ferguson DM, Moore DF, Getrich MA, Zhowandai MH. 2005. Enumeration and speciation of enterococci found in marine and intertidal sediments and coastal water in southern California. J. Appl. Microbiol.99:598-608.
4. Moore DF, Guzman JA, McGee C. 2008. Species distribution and antimicrobial resistance of enterococci isolated from surface and ocean water. J. Appl. Microbiol. 105:1017-1025.
5. American Public Health Association. 2005. Standard methods for the examination of water and wastewater, 21st ed. American Public Health Association, Washington, DC.
6. Facklam R, Elliott JA. 1995. Identification, classification, and clinical relevance of catalase-negative, Gram-positive cocci, excluding the streptococci and enterococci. Clin. Microbiol. Rev. 8:479-495.
7. Manero A, Vilanova X, Cerda-Cuellar M, Blanch AR. 2002. Characterization of sewage waters by biochemical fingerprinting of Enterococci. Water Res. 36:2831-2835.
8. Patel R, Piper KE, Rouse MS, Steckelberg JM, Uhl JR, Kohner P, Hopkins MK, Cockerill FR, Kline BC. 1998. Determination of 16S rRNA sequences of enterococci and application to species identification of nonmotile Enterococcus gallinarum isolates. J. Clin. Microbiol. 36:3399-3407.
9. Wheeler AL, Hartel PG, Godfrey DG, Hill JL, Segars WI. 2002. Potential of Enterococcus faecalis as a human fecal indicator for microbial source tracking. J. Environ. Qual. 31:1286-1293.
10. Schoen ME, Ashbolt NJ. 2010. Assessing pathogen risk to swimmers at non-sewage impacted recreational beaches. Environ. Sci. Technol. 44: 2286-2291.
11. Gardner TJ, Fitzgerald C, Xavier C, Klein R, Pruckler J, Stroika S, McLaughlin JB. 2011. Outbreak of campylobacteriosis associated with consumption of raw peas. Clin. Infect. Dis. 53:26-32.
12. Haugland RA, Siefring SC, Wymer LJ, Brenner KP, Dufour AP. 2005. Comparison of Enterococcus measurements in freshwater at two recreational beaches by quantitative polymerase chain reaction and membrane filter culture analysis. Water Res. 39:559-568.
13. Ludwig W, Schleifer KH. 2000. How quantitative is quantitative PCR with respect to cell counts? Syst. Appl. Microbiol. 23:556-562.
14. Maheux AF, Bissonnette L, Boissinot M, Bernier JL, Huppe V, Berube E, Boudreau DK, Picard FJ, Huletsky A, Bergeron MG. 2011. Method for rapid and sensitive detection of Enterococcus sp. and Enterococcus faecalis/faecium cells in potable water samples. Water Res. 45:2342-2354.
15. Messer JW, Dufour AP. 1998. A rapid, specific membrane filtration procedure for enumeration of enterococci in recreational water. Appl. Environ. Microbiol. 64:678-680.
16. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
17. Santo Domingo JW, Siefring SC, Haugland RA. 2003. Real-time PCR method to detect Enterococcus faecalis in water. Biotechnol. Lett. 25:261-265.
18. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
19. Ryu H, Tran H, Ware M, Iker B, Griffin S, Edge T, Newmann N, Villegas EN, Santo Domingo JW. 2011. Application of leftover sample material from waterborne protozoa monitoring for the molecular detection of Bacteroidales and fecal source tracking markers. J. Microbiol. Methods 86:337-343.
20. Ryu H, Griffith J, Hill S, Edge TA, Toledo-Hernandez C, Gonzalez- Nieves J, Santo Domingo JW. 2012. Comparison of gull feces-specific assays targeting the 16S rRNA genes of Catellicoccus marimammalium and Streptococcus spp. Appl. Environ. Microbiol. 78:1909-1916.
21. Jackson CR, Fedorka-Cray PJ, Barrett JB. 2004. Use of a genus- and species-specific multiplex PCR for identification of enterococci. J. Clin. Microbiol. 42:3558-3565.
22. Vermette CJ, Russell AH, Desai AR, Hill JE. 2010. Resolution of phenotypically distinct strains of Enterococcus spp. in a complex microbial community using cpn60 universal target sequencing. Microb. Ecol. 59:14-24.
23. Ahmed W, Sidhu JP, Toze S. 2012. Speciation and frequency of virulence genes of Enterococcus spp. isolated from rainwater tank samples in Southeast Queensland, Australia. Environ. Sci. Technol. 46:6843-6850.
24. Scott TM, Jenkins TM, Lukasik J, Rose JB. 2005. Potential use of a host associated molecular marker in Enterococcus faecium as an index of human fecal pollution. Environ. Sci. Technol. 39:283-287.
25. Mote BL, Turner JW, Lipp EK. 2012. Persistence and growth of the fecal indicator bacteria enterococci in detritus and natural estuarine plankton communities. Appl. Environ. Microbiol. 78:2569-2577.
26. Nayak BS, Badgley B, Harwood VJ. 2011. Comparison of genotypic and phylogenetic relationships of environmental Enterococcus isolates by BOX-PCR typing and 16S rRNA gene sequencing. Appl. Environ. Microbiol.77:5050-5055.
27. Grammenou P, Spiliopoulou I, Sazakli E, Papapetropoulou M. 2006. PFGE analysis of enterococci isolates from recreational and drinking water in Greece. J. Water Health 4:263-269.
28. Lleo MM, Bonato B, Tafi MC, Signoretto C, Boaretti M, Canepari P. 2001. Resuscitation rate in different enterococcal species in the viable butnon-culturable state. J. Appl. Microbiol. 91:1095-1102.
29. Layton BA, Walters SP, Lam LH, Boehm AB. 2010. Enterococcus species distribution among human and animal hosts using multiplex PCR. J. Appl. Microbiol. 109:539-547.
30. Maraccini PA, Ferguson DM, Boehm AB. 2012. Diurnal variation in Enterococcus species composition in polluted ocean water and a potential role for the enterococcal carotenoid in protection against photoinactivation. Appl. Environ. Microbiol. 78:305-310.
31. Viau E, Peccia J. 2009. Evaluation of the enterococci indicator in biosolids using culture-based and quantitative PCR assays. Water Res. 43:4878-4887.
32. Lu J, Santo Domingo JW, Lamendella R, Edge T, Hill S. 2008. Phylogenetic diversity and molecular detection of bacteria in gull feces. Appl. Environ. Microbiol. 74:3969-3976.
33. Frahm E, Obst U. 2003. Application of the fluorogenic probe technique (TaqMan PCR) to the detection of Enterococcus spp. and Escherichia coli in water samples. J. Microbiol. Methods 52:123-131.
34. U.S. EPA Office of Water. 2010. Method A: Enterococci in water by TaqMan® quantitative polymerase chain reaction (qPCR) assay. EPA-821-R-10-004. U.S. Environmental Protection Agency, Washington, DC.
35. Arvanitidou M, Katsouyannopoulos V, Tsakris A. 2001. Antibiotic resistance patterns of enterococci isolated from coastal bathing waters. J. Med. Microbiol. 50:1001-1005.
36. Svec P, Sedlacek I. 1999. Occurrence of Enterococcus spp. in waters. Folia Microbiol. (Praha) 44:3-10.
37. Suzuki Y, Kanda N, Furukawa T. 2012. Abundance of Enterococcus species, Enterococcus faecalis and Enterococcus faecium, essential indicators f fecal pollution, in river water. J. Environ. Sci. Health A Tox. Hazard. Subst. Environ. Eng. 47:1500-1505.
38. Svec P, Devriese LA, Sedlacek I, Baele M, Vancanneyt M, Haesebrouck F, Swings J, Doskar J. 2001. Enterococcus haemoperoxidus sp. nov. and Enterococcus moraviensis sp. nov., isolated from water. Int. J. Syst. Evol. Microbiol. 51:1567-1574.
39. Svec P, Vancanneyt M, Devriese LA, Naser SM, Snauwaert C, Lefebvre K, Hoste B, Swings J. 2005. Enterococcus aquimarinus sp. nov., isolated from sea water. Int. J. Syst. Evol. Microbiol. 55:2183-2187.
40. Svec P, Vancanneyt M, Koort J, Naser SM, Hoste B, Vihavainen E, Vandamme P, Swings J, Bjorkroth J. 2005. Enterococcus devriesei sp. nov., associated with animal sources. Int. J. Syst. Evol. Microbiol. 55:2479-2484.
41. Carvalho MdGS, Shewmaker PL, Steigerwalt AG, Morey RE, Sampson AJ, Joyce K, Barrett TJ, Teixeira LM, Facklam RR. 2006. Enterococcus caccae sp. nov., isolated from human stools. Int. J. Syst. Evol. Microbiol.56:1505-1508.
42. Naser SM, Vancanneyt M, De Graef E, Devriese LA, Snauwaert C, Lefebvre K, Hoste B, Svec P, Decostere A, Haesebrouck F, Swings J. 2005. Enterococcus canintestini sp. nov., from faecal samples of healthy dogs. Int. J. Syst. Evol. Microbiol. 55:2177-2182.
43. Gordon DM, Bauer S, Johnson JR. 2002. The genetic structure of Escherichia coli populations in primary and secondary habitats. Microbiology 148:1513-1522.