Intestinal microbiota and species diversity of Campylobacter and Helicobacter spp. in migrating shorebirds in Delaware Bay

Applied and Environmental Microbiology

Volumn 80, Issue 6, 2014, Pages 1838-1847

  Ryu, Hodon ^a   Grond, Kirsten ^b,c,d   Verheijen, Bram ^d   Elk, Michael ^a   Buehler, Deborah M ^b,c   Santo Domingo, Jorge W ^a  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^b DEPARTMENT OF NATURAL HISTORY   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d KANSAS STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA GENE SEQUENCING; BACTERIAL COMMUNITY; BACTERIAL DIVERSITY; BACTERIAL PATHOGENS; CAMPYLOBACTER SPECIES; FECAL INDICATOR BACTERIA; MICROBIAL COMMUNITIES; PATHOGENIC SPECIES;

GENES; LIBRARIES; POLYMERASE CHAIN REACTION; RNA;

CLONING;

BACTERIUM; MICROBIAL COMMUNITY; MIGRATORY SPECIES; PATHOGEN; SPECIES DIVERSITY; STOPOVER; WADER; WATERFOWL;

DELAWARE BAY; UNITED STATES;

BACTERIAL DNA; RIBOSOME DNA; RNA 16S;

ANIMAL; ARTICLE; BIOTA; CAMPYLOBACTER; CHARADRIIFORMES; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; FECES; GASTROINTESTINAL TRACT; GENETICS; HELICOBACTER; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PREVALENCE; REAL TIME POLYMERASE CHAIN REACTION; UNITED STATES;

ANIMALS; BIOTA; CAMPYLOBACTER; CHARADRIIFORMES; CLUSTER ANALYSIS; DELAWARE; DNA, BACTERIAL; DNA, RIBOSOMAL; FECES; GASTROINTESTINAL TRACT; HELICOBACTER; MOLECULAR SEQUENCE DATA; PHYLOGENY; PREVALENCE; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

EID: 84897621379     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03793-13     Document Type: Article

References (44)

1. Newman SH, Hill NJ, Spragens KA, Janies D, Voronkin IO, Prosser DJ, Yan B, Lei F, Batbayar N, Natsagdorj T, Bishop CM, Butler PJ, Wikelski M, Balachandran S, Mundkur T, Douglas DC, Takekawa JY. 2012. Eco-virological approach for assessing the role of wild birds in the spread of avian Influenza H5N1 along the central Asian flyway. PLoS One 7(2): e30636. http://dx.doi.org/10.1371/journal.pone.0030636.
2. Lawson B, Robinson RA, Neimanis A, Handeland K, Isomursu M, Agren EO, Hamnes IS, Tyler KM, Chantrey J, Hughes LA, Pennycott TW, Simpson VR, John SK, Peck KM, Toms MP, Bennett M, Kirkwood JK, Cunningham AA. 2011. Evidence of spread of the emerging infectious disease, finch trichomonosis, by migrating birds. EcoHealth 8:143-153. http://dx.doi.org/10.1007/s10393-011-0696-8.
3. Rvachev L, Longini I, Jr. 1985. A mathematical-model for the global spread of Influenza. Math. Biosci. 75:3-22. http://dx.doi.org/10.1016/0025-5564(85)90064-1.
4. Clark K, Niles L, Burger J. 1993. Abundance and distribution of migrant shorebirds in Delaware Bay. Condor 95:694-705. http://dx.doi.org/10.2307/1369612.
5. Jorgensen JG, McCarty JP, Wolfenbarger LL. 2008. Buff-breasted sandpiper density and numbers during migratory stopover in the Rainwater Basin, Nebraska. Condor 110:63-69. http://dx.doi.org/10.1525/cond.2008.110.1.63.
6. Camarda A, Circella E, Pennelli D, Madio A, Bruni G, Lagrasta V, Marzano G, Mallia E, Campagnari E. 2006. Wild birds as biological indicators of environmental pollution: biotyping and antimicrobial resistance patterns of Escherichia coli isolated from Audouin's gulls (Larus audouinii) living in the Bay of Gallipoli (Italy). Ital. J. Anim. Sci. 5:287-290. http://dx.doi.org/10.4081/ijas.2006.287.
7. Keller JI, Shriver WG, Waldenstrom J, Griekspoor P, Olsen B. 2011. Prevalence of Campylobacter in wild birds of the mid-Atlantic region, U.S.A. J. Wildl. Dis. 47:750-754. http://dx.doi.org/10.7589/0090-3558-47.3.750.
8. 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.
9. Ksoll WB, Ishii S, Sadowsky MJ, Hicks RE. 2007. Presence and sources of fecal coliform bacteria in epilithic periphyton communities of Lake Superior. Appl. Environ. Microbiol. 73:3771-3778. http://dx.doi.org/10.1128/AEM.02654-06.
10. Lu J, Santo Domingo JW, Hill S, Edge TA. 2009. Microbial diversity and host-specific sequences of Canada goose feces. Appl. Environ. Microbiol. 75:5919-5926. http://dx.doi.org/10.1128/AEM.00462-09.
11. Zhou L, Kassa H, Tischler ML, Xiao LH. 2004. Host-adapted Cryptosporidium spp. in Canada geese (Branta canadensis). Appl. Environ. Microbiol. 70:4211-4215. http://dx.doi.org/10.1128/AEM.70.7.4211-4215.2004.
12. Hudson CR, Quist C, Lee MD, Keyes KI, Dodson SV, Morales C, Sanchez S, White DG, Maurer JJ. 2000. Genetic relatedness of Salmonella isolates from nondomestic birds in southeastern United States. J. Clin. Microbiol. 38:1860-1865.
13. Blanco G, Lemus JA, Grande J. 2006. Faecal bacteria associated with different diets of wintering red kites: influence of livestock carcass dumps in microflora alteration and pathogen acquisition. J. Appl. Ecol. 43:990-998. http://dx.doi.org/10.1111/j.1365-2664.2006.01200.x.
14. Wither A, Rehfisch M, Austin G. 2005. The impact of bird populations on the microbiological quality of bathing waters. Water Sci. Technol. 51: 199-207.
15. Kilpatrick AM. 2011. Globalization, land use, and the invasion of West Nile virus. Science 334:323-327. http://dx.doi.org/10.1126/science.1201010.
16. Ulbert S. 2011. West Nile virus: the complex biology of an emerging pathogen. Intervirology 54:171-184. http://dx.doi.org/10.1159/000328320.
17. Rose M, Nol E. 2010. Foraging behavior of non-breeding semipalmated plovers. Waterbirds 33:59-69. http://dx.doi.org/10.1675/063.033.0107.
18. Santos SS, Pardal S, Proenca DN, Lopes RJ, Ramos JA, Mendes L, Morais PV. 2012. Diversity of cloacal microbial community in migratory shorebirds that use the Tagus estuary as stopover habitat and their potential to harbor and disperse pathogenic microorganisms. FEMS Microbiol. Ecol. 82:63-74. http://dx.doi.org/10.1111/j.1574-6941.2012.01407.x.
19. Hermans D, Pasmans F, Messens W, Martel A, Van Immerseel F, Rasschaert G, Heyndrickx M, Van Deun K, Haesebrouck F. 2012. Poultry as a host for the zoonotic pathogen Campylobacter jejuni. Vector-Borne Zoonotic Dis. 12:89-98. http://dx.doi.org/10.1089/vbz.2011.0676.
20. Waldenstrom J, On SLW, Ottvall R, Hasselquist D, Olsen B. 2007. Species diversity of campylobacteria in a wild bird community in Sweden. J. Appl. Microbiol. 102:424-432. http://dx.doi.org/10.1111/j.1365-2672.2006.03090.x.
21. Lu J, Ryu H, Santo Domingo JW, 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.
22. Lu J, Ryu H, Vogel J, Santo Domingo J, Ashbolt N. 2013. Molecular detection of Campylobacter and fecal indicators during the northern migration of sandhill cranes (Grus canadensis) at the Central Platte River. Appl. Environ. Microbiol. 79:3762-3769. http://dx.doi.org/10.1128/AEM.03990-12.
23. Wilson IG. 1997. Inhibition and facilitation of nucleic acid amplification. Appl. Environ. Microbiol. 63:3741-3751.
24. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI. 2008. Evolution of mammals and their gut microbes. Science 320:1647-1651. http://dx.doi.org/10.1126/science.1155725.
25. Rossmassler K, Engel AS, Twing KI, Hanson TE, Campbell BJ. 2012. Drivers of epsilonproteobacterial community composition in sulfidic caves and springs. FEMS Microbiol. Ecol. 79:421-432. http://dx.doi.org/10.1111/j.1574-6941.2011.01231.x.
26. Huber T, Faulkner G, Hugenholtz P. 2004. Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317-2319. http://dx.doi.org/10.1093/bioinformatics/bth226.
27. DeSantis TZ, Hugenholtz P, Keller K, Brodie EL, Larsen N, Piceno YM, Phan R, Andersen GL. 2006. NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res. 34:W394-W399. http://dx.doi.org/10.1093/nar/gkl244.
28. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. 2006. Greengenes, a chimerachecked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72:5069-5072. http://dx.doi.org/10.1128/AEM.03006-05.
29. 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.
30. Lund M, Nordentoft S, Pedersen K, Madsen M. 2004. Detection of Campylobacter spp. in chicken fecal samples by real-time PCR. J. Clin. Microbiol. 42:5125-5132. http://dx.doi.org/10.1128/JCM.42.11.5125-5132.2004.
31. Ludwig W, Schleifer KH. 2000. How quantitative is quantitative PCR with respect to cell counts? Syst. Appl. Microbiol. 23:556-562. http://dx.doi.org/10.1016/S0723-2020(00)80030-2.
32. Santo Domingo JW, Siefring SC, Haugland RA. 2003. Real-time PCR method to detect Enterococcus faecalis in water. Biotechnol. Lett. 25:261-265. http://dx.doi.org/10.1023/A:1022303118122.
33. Ryu H, Henson M, Elk M, Toledo-Hernandez C, Griffith J, Blackwood D, Noble R, Gourmelon M, Glassmeyer S, Santo Domingo J. 2013. Development of quantitative PCR assays targeting 16S rRNA gene 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.
34. Bustin SA, Vandesompele J, Pfaffl MW. 2009. Standardization of qPCR and RT-qPCR. Genet. Eng. Biotechnol. News 29:40-43. http://hdl.handle.net/1854/LU-876361.
35. Ryu H, Griffith JF, Khan IUH, Hill S, Edge TA, Toledo-Hernandez C, Gonzalez-Nieves J, Santo Domingo J. 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.
36. 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.
37. Fogarty LR, Voytek MA. 2005. Comparison of Bacteroides-Prevotella 16S rRNA genetic markers for fecal samples from different animal species. Appl. Environ. Microbiol. 71:5999-6007. http://dx.doi.org/10.1128/AEM.71.10.5999-6007.2005.
38. Jeter SN, McDermott CM, Bower PA, Kinzelman JL, Bootsma MJ, Goetz GW, McLellan SL. 2009. Bacteroidales diversity in ring-billed gulls (Larus delawarensis) residing at Lake Michigan beaches. Appl. Environ. Microbiol. 75:1525-1533. http://dx.doi.org/10.1128/AEM.02261-08.
39. Ryu H, Lu J, Vogel J, Elk M, Chavez-Ramirez F, Ashbolt N, Santo Domingo J. 2012. Development and evaluation of a quantitative PCR assay targeting sandhill crane (Grus canadensis) fecal pollution. Appl. Environ. Microbiol. 78:4338-4345. http://dx.doi.org/10.1128/AEM.07923-11.
40. 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): e00019-12. http://dx.doi.org/10.1128/genomeA.00019-12.
41. Waldenström J, Broman T, Carlsson I, Hasselquist D, Achterberg RP, Wagenaar JA, Olsen B. 2002. Prevalence of Campylobacter jejuni, Campylobacter lari, and Campylobacter coli in different ecological guilds and taxa of migrating birds. Appl. Environ. Microbiol. 68:5911-5917. http://dx.doi.org/10.1128/AEM.68.12.5911-5917.2002.
42. Rosef O, Gondrosen B, Kapperud G, Underdal B. 1983. Isolation and characterization of Campylobacter jejuni and Campylobacter coli from domestic and wild mammals in Norway. Appl. Environ. Microbiol. 46:855-859.
43. Coker AO, Isokpehi RD, Thomas BN, Amisu KO, Obi CL. 2002. Human campylobacteriosis in developing countries. Emerg. Infect. Dis. 8:237-243. http://dx.doi.org/10.3201/eid0803.010233.
44. Samuel MC, Vugia DJ, Shallow S, Marcus R, Segler S, McGivern T, Kassenborg H, Reilly K, Kennedy M, Angulo F, Tauxe RV. 2004. Epidemiology of sporadic Campylobacter infection in the United States and declining trend in incidence, FoodNet 1996-1999. Clin. Infect. Dis. 38:S165-S174. http://dx.doi.org/10.1086/381583.