Analysis of the Gull Fecal Microbial Community Reveals the Dominance of Catellicoccus marimammalium in Relation to Culturable Enterococci

Applied and Environmental Microbiology

Volumn 80, Issue 2, 2014, Pages 757-765

  Koskey, Amber M ^a   Fisher, Jenny C ^a   Traudt, Mary F ^a   Newton, Ryan J ^a   McLellan, Sandra L ^a  

^a UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA GENE SEQUENCE; 16S RRNA GENE SEQUENCING; ENTEROBACTERIACEAE; ENTEROCOCCUS SPP; FECAL CONTAMINATION; FECAL INDICATOR BACTERIA; MICROBIAL COMMUNITIES; SEQUENCE COMPARISONS;

BEACHES; ESCHERICHIA COLI; MICROORGANISMS; RNA; WATER POLLUTION;

GENES;

ABUNDANCE; BEACH; COLIFORM BACTERIUM; DOMINANCE; GENETIC MARKER; MICROBIAL COMMUNITY; SAMPLING;

RNA 16S;

ANIMAL; ARTICLE; CHARADRIIFORMES; CLASSIFICATION; ENTEROBACTERIACEAE; ENTEROCOCCACEAE; ENVIRONMENTAL MONITORING; FECES; GASTROINTESTINAL TRACT; GENETICS; HIGH THROUGHPUT SEQUENCING; ISOLATION AND PURIFICATION; LAKE; METHODOLOGY; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; REPRODUCIBILITY; UNITED STATES;

ANIMALS; BACTERIOLOGICAL TECHNIQUES; CHARADRIIFORMES; ENTEROBACTERIACEAE; ENTEROCOCCACEAE; ENVIRONMENTAL MONITORING; FECES; GASTROINTESTINAL TRACT; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; LAKES; MOLECULAR SEQUENCE DATA; PHYLOGENY; REPRODUCIBILITY OF RESULTS; RNA, RIBOSOMAL, 16S; WISCONSIN;

EID: 84892458139     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02414-13     Document Type: Article

References (44)

1. Alderisio KA, DeLuca N. 1999. Seasonal enumeration of fecal coliform bacteria from the feces of ring-billed gulls (Larus delawarensis) and Canada geese (Branta canadensis). Appl. Environ. Microbiol. 65:5628-5630.
2. Converse RR, Kinzelman JL, Sams EA, Hudgens E, Dufour AP, Ryu H, Santo-Domingo JW, Kelty CA, Shanks OC, Siefring SD, Haugland RA, Wade TJ. 2012. Dramatic improvements in beach water quality following gull removal. Environ. Sci. Technol. 46:10206-10213. http://dx.doi.org/10.1021/es302306b.
3. Fogarty LR, Haack SK, Wolcott MJ, Whitman RL. 2003. Abundance and characteristics of the recreational water quality indicator bacteria Escherichia coli and enterococci in gull faeces. J. Appl. Microbiol. 94:865-878. http://dx.doi.org/10.1046/j.1365-2672.2003.01910.x.
4. Lévesque B, Brousseau P, Simard P, Dewailly E, Meisels M, Ramsay D, Joly J. 1993. Impact of the ring-billed gull (Larus delawarensis) on the microbiological quality of recreational water. Appl. Environ. Microbiol. 59:1228-1230.
5. Meerburg BG, Koene MG, Kleijn D. 2011. Escherichia coli concentrations in feces of geese, coots, and gulls residing on recreational water in The Netherlands. Vector Borne Zoonotic Dis. 11:601-603. http://dx.doi.org/10.1089/vbz.2010.0218.
6. US Environmental Protection Agency. 1986. Ambient water quality criteria for bacteria. Office of Water, Regulation and Standards, US Environmental Protection Agency, Washington, DC.
7. McLellan SL, Boehm AB, Shanks OC. 2013. Marine and freshwater fecal indicators and source identification, p 199-236. In Kanki P, Grimes DJ (ed), Infectious diseases: selected entries from the encyclopedia of sustainability science and technology. Springer Science Business Media, New York, NY.
8. Albarnaz JD, Toso J, Correa AA, Simoes CMO, Barardi CRM. 2007. Relationship between the contamination of gulls (Larus dominicanus) and oysters (Crassostrea gigas) with Salmonella serovar Typhimurium by PCRRFLP. Int. J. Environ. Health Res. 17:133-140. http://dx.doi.org/10.1080/09603120701219816.
9. Kinzelman J, McLellan SL, Amick A, Preedit J, Scopel CO, Olapade O, Gradus S, Singh A, Sedmak G. 2008. Identification of human enteric pathogens in gull feces at Southwestern Lake Michigan bathing beaches. Can. J. Microbiol. 54:1006-1015. http://dx.doi.org/10.1139/W08-096.
10. Lu JR, Ryu H, Domingo JWS, Griffith JF, Ashbolt N. 2011. Molecular detection of Campylobacter spp. in California gull (Larus californicus) excreta. Appl. Environ. Microbiol. 77:5034-5039. http://dx.doi.org/10.1128/AEM.00018-11.
11. Quessy S, Messier S. 1992. Prevalence of Salmonella spp., Campylobacter spp. and Listeria spp. in ring-billed gulls (Larus delawarensis). J. Wildl. Dis. 28:526-531. http://dx.doi.org/10.7589/0090-3558-28.4.526.
12. Schoen ME, Ashbolt NJ. 2010. Assessing pathogen risk to swimmers at non-sewage impacted recreational beaches. Environ. Sci. Technol. 44: 2286-2291. http://dx.doi.org/10.1021/es903523q.
13. Soller JA, Schoen ME, Bartrand T, Ravenscroft JE, Ashbolt NJ. 2010. Estimated human health risks from exposure to recreational waters impacted by human and non-human sources of faecal contamination. Water Res. 44:4674-4691. http://dx.doi.org/10.1016/j.watres.2010.06.049.
14. Rabinovici SJM, Bernknopf R, Wein A. 2004. Economics and health risk trade-offs of swim closures at a Lake Michigan beach. Environ. Sci. Technol. 38:2737-2745. http://dx.doi.org/10.1021/es034905z.
15. Edge TA, Hill S. 2007. Multiple lines of evidence to identify the sources of fecal pollution at a freshwater beach in Hamilton Harbour, Lake Ontario. Water Res. 41:3585-3594. http://dx.doi.org/10.1016/j.watres.2007.05.012.
16. US Environmental Protection Agency. 2002. National beach guidance and required performance criteria for grants EPA-823-B-02-004. Office of Water, US Environmental Protection Agency, Washington, DC.
17. Engeman RM, Hartmann JW, Beckerman SF, Seamans TW, Abu-Absi S. 2012. Egg oiling to reduce hatch-year ring-billed gull numbers on Chicago's beaches during swim season and water quality test results. Eco- Health 9:195-204. http://dx.doi.org/10.1007/s10393-012-0760-z.
18. Hartmann JW, Beckerman SF, Seamans TW, Engeman RM, Abu- Absi S. 8 February 2013. Report to the City of Chicago on Conflicts with Ring-Billed Gulls and the 2012 Integrated Ring-Billed Gull Damage Management Project. http://www.aphis.usda.gov/wildlife_damage/nwrc/publications/13pubs/engeman134.pdf.
19. Sauer JR, Hines JE, Fallon J. 2008. The North American breeding bird survey, results and analysis 1966-2007. Version 5.15.2008. USGS Patuxent Wildlife Research Center, Laurel, MD. http://www.mbr-pwrc.usgs.gov/bbs/bbs2007.html.
20. Jeter SN, McDermott CM, Bower PA, Kinzelman JL, Bootsma MJ, Goetz GW, McLellan SL. 2009. Bacteroidales diversity in ring-billed gulls (Laurus delawarensis) residing at Lake Michigan beaches. Appl. Environ. Microbiol. 75:1525-1533. http://dx.doi.org/10.1128/AEM.02261-08.
21. 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. http://dx.doi.org/10.1128/AEM.00019-08.
22. Ryu H, Griffith JF, Khan IU, Hill S, Edge TA, Toledo-Hernandez C, Gonzalez-Nieves J, Santo Domingo JW. 2012. Comparison of gull fecesspecific assays targeting the 16S rRNA genes of Catellicoccus marimammalium and Streptococcus spp. Appl. Environ. Microbiol. 78:1909-1916. http://dx.doi.org/10.1128/AEM.07192-11.
23. Huse SM, Dethlefsen L, Huber JA, Welch DM, Relman DA, Sogin ML. 2008, Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet. 4:e1000255. http://dx.doi.org/10.1371/journal.pgen.1000255.
24. Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, Herndl GJ. 2006. Microbial diversity in the deep sea and the underexplored "rare biosphere". Proc. Nat. Acad. Sci. U. S. A. 103:12115- 12120. http://dx.doi.org/10.1073/pnas.0605127103.
25. Lee C, Marion J, Lee J. 2013. Development and application of a quantitative PCR assay targeting Catellicoccus marimammalium for assessing gull-associated fecal contamination at Lake Erie beaches. Sci. Total Environ. 454-455:1-8.
26. Sinigalliano CD, Ervin JS, Van De Werfhorst LC, Badgley BD, Balleste E, Bartkowiak J, Boehm AB, Byappanahalli M, Goodwin KD, Gourmelon M, Griffith J, Holden PA, Jay J, Layton B, Lee C, Lee J, Meijer WG, Noble R, Raith M, Ryu H, Sadowsky MJ, Schriewer A, Wang D, Wanless D, Whitman R, Wuertz S, Santo Domingo JW. 5 July 2013. Multi-laboratory evaluation of the performance of Catellicoccus marimammalium PCR assays developed to target gull fecal sources. Water Res. http://dx.doi.org/10.1016/j.watres.2013.02.059.
27. Marteinsson VT, Runarsson A, Stefansson A, Thorsteinsson T, Johannesson T, Magnusson SH, Reynisson E, Einarsson B, Wade N, Morrison HG, Gaidos E. 2013. Microbial communities in the subglacial waters of the Vatnajokull ice cap, Iceland. ISME J. 7:427-437. http://dx.doi.org/10.1038/ismej.2012.97.
28. Morrison H, Grim S, Vineis J, Sogin M. 2013. 16S amplicon fusion primers and protocol for Illumina platform sequencing. figshare. http://dx.doi.org/10.6084/m9.figshare.833944.
29. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541. http://dx.doi.org/10.1128/AEM.01541-09.
30. Wright ES, Yilmaz LS, Noguera DR. 2012. DECIPHER, a search-based approach to chimera identification for 16S rRNA sequences. Appl. Environ. Microbiol. 78:717-725. http://dx.doi.org/10.1128/AEM.06516-11.
31. Wang Q, Garrity GM, Tiedje JM, Cole JR. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261-5267. http://dx.doi.org/10.1128/AEM.00062-07.
32. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
33. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739. http://dx.doi.org/10.1093/molbev/msr121.
34. US Environmental Protection Agency. 2002. Method 1600: enterococci in water by membrane filtration using membrane-Enterococcus indoxyl- β-D-glucoside agar (mEI). EPA 821-R-02-022. Office of Water, US Environmental Protection Agency, Washington, DC.
35. Dick LK, Bernhard AE, Brodeur TJ, Santo Domingo JW, Simpson JM, Walters SP, Field KG. 2005. Host distributions of uncultivated fecal Bacteroidales bacteria reveal genetic markers for fecal source identification. Appl. Environ. Microbiol. 71:3184-3191. http://dx.doi.org/10.1128/AEM.71.6.3184-3191.2005.
36. Kumar PS, Brooker MR, Dowd SE, Camerlengo T. 2011. Target region selection is a critical determinant of community fingerprints generated by 16S pyrosequencing. PLoS One 6:e20956. http://dx.doi.org/10.1371/journal.pone.0020956.
37. Chakravorty S, Helb D, Burday M, Connell N, Alland D. 2007. A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. J. Microbiol. Methods 69:330-339. http://dx.doi.org/10.1016/j.mimet.2007.02.005.
38. Bonilla TD, Nowosielski K, Esiobu N, McCorquodale DS, Rogerson A. 2006 Species assemblages of Enterococcus indicate potential sources of fecal bacteria at a south Florida recreational beach. Mar. Pollut. Bull. 52: 807-810. http://dx.doi.org/10.1016/j.marpolbul.2006.03.003.
39. 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. http://dx.doi.org/10.1128/AEM.06902-11.
40. 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.
41. Lee ZM, Bussema C, Schmidt TM. 2009. rrnDB: documenting the number of rRNA and tRNA genes in bacteria and archaea. Nucleic Acids Res. 37:D489-D493. http://dx.doi.org/10.1093/nar/gkn689.
42. Weigand MR, Ryu H, Bozcek L, Konstantinidis KT, Santo Domingo JW. 2013. Draft genome sequence of Catellicoccus marimammalium, a novel species commonly found in gull feces. Genome Announc. 1(1): e00019-00012. http://dx.doi.org/10.1128/genomeA.00019-12.
43. Ryu H, Henson M, Elk M, Toledo-Hernandez C, Griffith J, Blackwood D, Noble R, Gourmelon M, Glassmeyer S, Santo Domingo JW. 2013. 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. Appl. Environ. Microbiol. 79:196-204. http://dx.doi.org/10.1128/AEM.02802-12.
44. Amann RI, Ludwig W, Schleifer KH. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59:143-169.