Microbial Ecology

, Volume 74, Issue 2, pp 496–506 | Cite as

Intestinal Microbial Community Dynamics of White-Tailed Deer (Odocoileus virginianus) in an Agroecosystem

  • M. Lisette Delgado
  • Pallavi Singh
  • Julie A. Funk
  • Jennifer A. Moore
  • Emily M. Cannell
  • Jeannette Kanesfsky
  • Shannon D. Manning
  • Kim T. Scribner
Host Microbe Interactions

Abstract

The intestinal microbiota has important functions that contribute to host health. The compositional dynamics of microbial communities are affected by many factors, including diet and presence of pathogens. In contrast to humans and domestic mammals, the composition and seasonal dynamics of intestinal microbiota of wildlife species remain comparatively understudied. White-tailed deer (Odocoileus virginianus) is an ecologically and economically important wildlife species that inhabits agricultural ecosystems and is known to be a reservoir of enteric pathogens. Nevertheless, there is a lack of knowledge of white-tailed deer intestinal microbiota diversity and taxonomic composition. This study’s first objective was to characterize and compare the intestinal microbiota of 66 fecal samples from white-tailed deer collected during two sampling periods (March and June) using 16S rDNA pyrosequencing. Associations between community diversity and composition and factors including season, sex, host genetic relatedness, and spatial location were quantified. Results revealed that white-tailed deer intestinal microbiota was predominantly comprised of phyla Firmicutes and Proteobacteria, whose relative frequencies varied significantly between sampling periods. The second objective was to examine the associations between the presence of Escherichia coli and Salmonella, and microbiota composition and diversity. Results indicated that relative abundance of some microbial taxa varied when a pathogen was present. This study provides insights into microbial compositional dynamics of a wildlife species inhabiting coupled natural and agricultural landscapes. Data focus attention on the high prevalence of Proteobacteria particularly during the summer and highlight the need for future research regarding the role of white-tailed deer as a natural pathogen reservoir in agroecosystems.

Keywords

Microbiota White-tailed deer 16S rRNA Pyrosequencing Agroecosystems Enteric pathogens 

Notes

Acknowledgments

This project was funded by the US Department of Agriculture (Project number 2011-67005-30004) and the W.K. Kellogg Foundation. This is publication 1991 from the Kellogg Biological Station. We would like to thank Jacquelyn Del_Valle, Rebekah E. Mosci, and Lindsey Ouellette for the sample collection and pathogen detection; the Fulbright commission from Peru, the Office for International Students and Scholars (OISS) from Michigan State University, and the National Institutes of Health Merial Scholars Program for the student funding.

Supplementary material

248_2017_961_MOESM1_ESM.docx (1.1 mb)
ESM 1 (DOCX 1165 kb).

References

  1. 1.
    Borer ET, Kinkel LL, May G, Seabloom EW (2013) The world within: quantifying the determinants and outcomes of a host’s microbiome. Basic Appl Ecol 14:533–539. doi: 10.1016/j.baae.2013.08.009 CrossRefGoogle Scholar
  2. 2.
    Shafquat A, Joice R, Simmons SL, Huttenhower C (2014) Functional and phylogenetic assembly of microbial communities in the human microbiome. Trends Microbiol. 22:261–266. doi: 10.1016/j.tim.2014.01.011 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    El Aidy S, Van Den Abbeele P, Van De Wiele T, et al (2013) Intestinal colonization: how key microbial players become established in this dynamic process: microbial metabolic activities and the interplay between the host and microbes prospects & overviews. S E. Aidy et al. BioEssays 35:913–923. doi: 10.1002/bies.201300073 Google Scholar
  4. 4.
    Leser TD, Mølbak L (2009) Better living through microbial action: the benefits of the mammalian gastrointestinal microbiota on the host. Environ. Microbiol. 11:2194–2206. doi: 10.1111/j.1462-2920.2009.01941.x CrossRefPubMedGoogle Scholar
  5. 5.
    Gu S, Chen D, Zhang J-N, et al (2013) Bacterial community mapping of the mouse gastrointestinal tract. PLoS One 8:e74957. doi: 10.1371/journal.pone.0074957 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Durso LM, Harhay GP, Smith TPL, et al (2010) Animal-to-animal variation in fecal microbial diversity among beef cattle. Appl. Environ. Microbiol. 76:4858–4862. doi: 10.1128/AEM.00207-10 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Singh P, Teal TK, Marsh TL, et al (2015a) Intestinal microbial communities associated with acute enteric infections and disease recovery. Microbiome 3:45. doi: 10.1186/s40168-015-0109-2 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Singh P, Sha Q, Lacher DW, et al (2015b) Characterization of enteropathogenic and Shiga toxin-producing Escherichia coli in cattle and deer in a shared agroecosystem. Front. Cell. Infect. Microbiol. doi: 10.3389/fcimb.2015.00029 Google Scholar
  9. 9.
    Dahllöf I (2002) Molecular community analysis of microbial diversity. Curr. Opin. Biotechnol. 13:213–217. doi: 10.1016/S0958-1669(02)00314-2 CrossRefPubMedGoogle Scholar
  10. 10.
    Carroll IM, Ringel-Kulka T, Siddle JP, et al (2012) Characterization of the fecal microbiota using high-throughput sequencing reveals a stable microbial community during storage. PLoS One 7:1–7. doi: 10.1371/journal.pone.0046953 Google Scholar
  11. 11.
    Coyte KZ, Schluter J, Foster KR (2015) The ecology of the microbiome: networks, competition, and stability. Science 350(80):663–666. doi: 10.1126/science.aad2602 CrossRefPubMedGoogle Scholar
  12. 12.
    Kamada N, Chen GY, Inohara N, Núñez G (2013) Control of pathogens and pathobionts by the gut microbiota. Nat. Immunol. 14:685–690. doi: 10.1038/ni.2608 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Zhao L, Tyler J, Starnes J, et al (2013) Correlation analysis of Shiga toxin-producing Escherichia coli shedding and faecal bacterial composition in beef cattle. J. Appl. Microbiol. 115:591–603CrossRefPubMedGoogle Scholar
  14. 14.
    Nelson KE, Zinder SH, Hance I, et al (2003) Phylogenetic analysis of the microbial populations in the wild herbivore gastrointestinal tract: insights into an unexplored niche. Environ. Microbiol. 5:1212–1220. doi: 10.1046/j.1462-2920.2003.00526.x CrossRefPubMedGoogle Scholar
  15. 15.
    Dostaler S, Ouellet JP, Therrien JF, Côté SD (2011) Are feeding preferences of white-tailed deer related to plant constituents? J. Wildl. Manag. 75:913–918. doi: 10.1002/jwmg.118 CrossRefGoogle Scholar
  16. 16.
    Renter DG, Sargeant JM, Hygnstorm SE, et al (2001) Escherichia coli O157:H7 in free-ranging deer in Nebraska. J. Wildl. Dis. 37:755–760CrossRefPubMedGoogle Scholar
  17. 17.
    Branham LA, Carr MA, Scott C, Callaway TR (2005) E. coli O157 and salmonella spp. in white-tailed deer and livestock. Curr Issues Intest Microbiol 6:25–29PubMedGoogle Scholar
  18. 18.
    Renter DG, Gnad DP, Sargeant JM, Hygnstrom SE (2006) Prevalence and serovars of Salmonella in the feces of free-ranging white-tailed deer (Odocoileus virginianus) in Nebraska. J. Wildl. Dis. 42:699–703. doi: 10.7589/0090-3558-42.3.699 CrossRefPubMedGoogle Scholar
  19. 19.
    Cleaveland S, Laurenson MK, Taylor LH (2001) Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 356:991–999. doi: 10.1098/rstb.2001.0889 CrossRefGoogle Scholar
  20. 20.
    Hofmann RR (1989) Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia 78:443–457. doi: 10.1007/BF00378733 CrossRefPubMedGoogle Scholar
  21. 21.
    Gruninger RJ, Sensen CW, TA MA, Forster RJ (2014) Diversity of rumen bacteria in Canadian cervids. PLoS One 9:1–9. doi: 10.1371/journal.pone.0089682 Google Scholar
  22. 22.
    Li Z, Zhang Z, Xu C, et al (2014) Bacteria and methanogens differ along the gastrointestinal tract of Chinese roe deer (Capreolus pygargus). PLoS One 9:e114513. doi: 10.1371/journal.pone.0114513 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Li ZP, Liu HL, Jin CA, et al (2013) Differences in the methanogen population exist in sika deer (Cervus nippon) fed different diets in China. Microb. Ecol. 66:879–888. doi: 10.1007/s00248-013-0282-4 CrossRefPubMedGoogle Scholar
  24. 24.
    Sundset MA, Edwards JE, Cheng YF, et al (2009) Molecular diversity of the rumen microbiome of norwegian reindeer on natural summer pasture. Microb. Ecol. 57:335–348. doi: 10.1007/s00248-008-9414-7 CrossRefPubMedGoogle Scholar
  25. 25.
    Dominianni C, Wu J, Hayes RB, Ahn J (2014) Comparison of methods for fecal microbiome biospecimen collection. BMC Microbiol. 14:103. doi: 10.1186/1471-2180-14-103 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Bahl MI, Bergström A, Licht TR (2012) Freezing fecal samples prior to DNA extraction affects the Firmicutes to Bacteroidetes ratio determined by downstream quantitative PCR analysis. FEMS Microbiol. Lett. 329:193–197. doi: 10.1111/j.1574-6968.2012.02523.x CrossRefPubMedGoogle Scholar
  27. 27.
    Kirkpatrick BW (1992) Identification of a conserved microsatellite site in the porcine and bovine insulin-like growth factor-I gene 5′ flank. Anim. Genet. 23:543–548CrossRefPubMedGoogle Scholar
  28. 28.
    Moore SS, Barendse W, Berger KT, et al (1992) Bovine and ovine DNA microsatellites from the EMBL and GENBANK databases. Anim. Genet. 23:463–467CrossRefPubMedGoogle Scholar
  29. 29.
    De Woody JA, Honeycutt RL, Skow LC (1995) Microsatellite markers in white-tailed deer. J Hered 86:317–319CrossRefGoogle Scholar
  30. 30.
    Wilson GA, Strobeck C, Wu L, Coffin JW (1997) Characterization of microsatellite loci in caribou Rangifer tarandus, and their use in other artiodactyls. Mol. Ecol. 6:697–699. doi: 10.1046/j.1365-294X.1997.00237.x CrossRefPubMedGoogle Scholar
  31. 31.
    Grear DA, Samuel MD, Scribner KT, et al (2010) Influence of genetic relatedness and spatial proximity on chronic wasting disease infection among female white-tailed deer. J. Appl. Ecol. 47:532–540. doi: 10.1111/j.1365-2664.2010.01813.x CrossRefGoogle Scholar
  32. 32.
    Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16:1099–1106. doi: 10.1111/j.1365-294X.2007.03089.x CrossRefPubMedGoogle Scholar
  33. 33.
    Lindsay AR, Belant JL (2008) A simple and improved PCR-based technique for white-tailed deer (Odocoileus virginianus) sex identification. Conserv. Genet. 9:443–447. doi: 10.1007/s10592-007-9326-y CrossRefGoogle Scholar
  34. 34.
    Trabulsi LR, Keller R, Gomes TAT (2002) Typical and atypical enteropathogenic Escherichia coli. Emerg. Infect. Dis. 8:508–513. doi: 10.3201/eid0805.010385 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Davies PR, Turkson PK, Funk JA, et al (2000) Comparison of methods for isolating Salmonella bacteria from faeces of naturally infected pigs. J. Appl. Microbiol. 89:169–177. doi: 10.1046/j.1365-2672.2000.01101.x CrossRefPubMedGoogle Scholar
  36. 36.
    Caporaso JG, Kuczynski J, Stombaugh J, et al (2010) Correspondence QIIME allows analysis of high-throughput community sequencing data intensity normalization improves color calling in SOLiD sequencing. Nat. Methods 7:335–336. doi: 10.1038/nmeth0510-335 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Edgar RC, Haas BJ, Clemente JC, et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi: 10.1093/bioinformatics/btr381 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    DeSantis TZ, Hugenholtz P, Larsen N, et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72:5069–5072. doi: 10.1128/AEM.03006-05 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Segata N, Izard J, Waldron L, et al (2011) Metagenomic biomarker discovery and explanation. Genome Biol. 12:R60. doi: 10.1186/gb-2011-12-6-r60 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6:288–295. doi: 10.1111/j.1471-8286.2005.01155.x CrossRefGoogle Scholar
  41. 41.
    Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539. doi: 10.1093/bioinformatics/bts460
  42. 42.
    Tamura K, Stecher G, Peterson D, et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30:2725–2729. doi: 10.1093/molbev/mst197 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res. 27:209–220PubMedGoogle Scholar
  44. 44.
    Mukhopadhya I, Hansen R, El-Omar EM, Hold GL (2012) IBD—what role do Proteobacteria play? Nat Rev Gastroenterol Hepatol 9:219–230. doi: 10.1038/nrgastro.2012.14 CrossRefPubMedGoogle Scholar
  45. 45.
    Reeves AE, Theriot CM, Bergin IL, et al (2011) The interplay between microbiome dynamics and pathogen dynamics in a murine model of Clostridium difficile infection. Gut Microbes 2:145–158. doi: 10.4161/gmic.2.3.16333 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Grønvold AMR, Mao Y, L’Abée-Lund TM, et al (2011) Fecal microbiota of calves in the clinical setting: effect of penicillin treatment. Vet. Microbiol. 153:354–360. doi: 10.1016/j.vetmic.2011.05.040 CrossRefPubMedGoogle Scholar
  47. 47.
    De Menezes AB, Lewis E, O’Donovan M, et al (2011) Microbiome analysis of dairy cows fed pasture or total mixed ration diets. FEMS Microbiol. Ecol. 78:256–265. doi: 10.1111/j.1574-6941.2011.01151.x CrossRefPubMedGoogle Scholar
  48. 48.
    Edrington TS, Callaway TR, Ives SE, et al (2006) Seasonal shedding of O157:H7 in ruminants: a new hypothesis. Foodborne Pathog. Dis. 3:413–421CrossRefPubMedGoogle Scholar
  49. 49.
    Magle SB, Kardash LH, Rothrock AO, et al (2015) Movements and habitat interactions of white-tailed deer: implications for chronic wasting disease management. Am. Midl. Nat. 173:267–282. doi: 10.1674/amid-173-02-267-282.1 CrossRefGoogle Scholar
  50. 50.
    Jenks J, Leslie D, Lochmiller R, Melchiors M (1994) Variation in gastrointestinal characteristics of male and female white-tailed deer: implications for resource partitioning. J. Mammal. 75:1045–1053CrossRefGoogle Scholar
  51. 51.
    Banks JC, Cary SC, Hogg ID (2009) The phylogeography of Adelie penguin faecal flora. Environ. Microbiol. 11:577–588. doi: 10.1111/j.1462-2920.2008.01816.x CrossRefPubMedGoogle Scholar
  52. 52.
    Goldberg E, Amir I, Zafran M, et al (2014) The correlation between Clostridium-difficile infection and human gut concentrations of Bacteroidetes phylum and clostridial species. Eur. J. Clin. Microbiol. Infect. Dis. 33:377–383. doi: 10.1007/s10096-013-1966-x CrossRefPubMedGoogle Scholar
  53. 53.
    Callaway TR, Edrington TS, Loneragan GH, et al (2013) Shiga Toxin-Producing Escherichia coli (STEC) ecology in cattle and management based options for reducing fecal shedding. 3Google Scholar
  54. 54.
    Dong HJ, Kim W, An JU, et al (2016) The fecal microbial communities of dairy cattle shedding Shiga toxin–producing Escherichia coli or campylobacter jejuni. Foodborne Pathog. Dis. 13:502–508. doi: 10.1089/fpd.2016.2121 CrossRefPubMedGoogle Scholar
  55. 55.
    Abu-Ali GS, Lacher DW, Wick LM, et al (2009) Genomic diversity of pathogenic Escherichia coli of the EHEC 2 clonal complex. BMC Genomics 10:296. doi: 10.1186/1471-2164-10-296 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Ahmer BMM, Gunn JS (2011) Interaction of Salmonella spp. with the intestinal microbiota. Front. Microbiol. 2:1–9. doi: 10.3389/fmicb.2011.00101 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • M. Lisette Delgado
    • 1
  • Pallavi Singh
    • 2
  • Julie A. Funk
    • 3
  • Jennifer A. Moore
    • 4
  • Emily M. Cannell
    • 1
  • Jeannette Kanesfsky
    • 1
  • Shannon D. Manning
    • 2
  • Kim T. Scribner
    • 1
  1. 1.Department of Fisheries and WildlifeMichigan State UniversityEast LansingUSA
  2. 2.Department of Microbiology and Molecular GeneticsMichigan State UniversityEast LansingUSA
  3. 3.College of Veterinary MedicineMichigan State UniversityEast LansingUSA
  4. 4.Department of BiologyGrand Valley State UniversityAllendaleUSA

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