1887

Abstract

There is increasing recognition that microbiomes are important for host health and ecology, and understanding host microbiomes is important for planning appropriate conservation strategies. However, microbiome data are lacking for many taxa, including turtles. To further our understanding of the interactions between aquatic microbiomes and their hosts, we used next generation sequencing technology to examine the microbiomes of the Krefft’s river turtle (). We examined the microbiomes of the buccal (oral) cavity, skin on the head, parts of the shell with macroalgae and parts of the shell without macroalgae. Bacteria in the phyla and were the most common in most samples (particularly buccal samples), but , and were also common (particularly in external microbiomes). We found significant differences in community composition among each body area, as well as significant differences among individuals. The buccal cavity had lower bacterial richness and evenness than any of the external microbiomes, and it had many amplicon sequence variants (ASVs) with a low relative abundance compared to other body areas. Nevertheless, the buccal cavity also had the most unique ASVs. Parts of the shell with and without algae also had different microbiomes, with particularly obvious differences in the relative abundances of the families , and . This study provides novel, baseline information about the external microbiomes of turtles and is a first step in understanding their ecological roles.

Funding
This study was supported by the:
  • Donald T McKnight , Australian Wildlife Society , (Award NA)
  • Donald T McKnight , Australian Society of Herpetologists , (Award NA)
  • Donald T McKnight , Skyrail Rainforest Foundation , (Award NA)
  • Donald T McKnight , Holsworth Wildlife Research Endowment , (Award NA)
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2020-03-26
2020-04-03
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References

  1. Mattoso TC, Moreira DDO, Samuels RI. Symbiotic bacteria on the cuticle of the leaf-cutting ant Acromyrmex subterraneus subterraneus protect workers from attack by entomopathogenic fungi. Biol Lett 2011; 8: 461 464
    [Google Scholar]
  2. Harris RN, Brucker RM, Walke JB, Becker MH, Schwantes CR et al. Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. Isme J 2009; 3: 818 824
    [Google Scholar]
  3. Mao-Jones J, Ritchie KB, Jones LE, Ellner SP. How microbial community composition regulates coral disease development. PLoS Biol 2010; 8: e1000345
    [Google Scholar]
  4. Appril A. Marine animal microbiomes: toward understanding Host-microbiome interactions in a changing Ocean. Front Mar Sci 2017; 4: 222
    [Google Scholar]
  5. West AG, Waite DW, Deines P, Bourne DG, Digby A et al. The microbiome in threatened species conservation. Biol Conserv 2019; 229: 85 98
    [Google Scholar]
  6. Redford KH, Segre JA, Salafsky N, del Rio CM, McAloose D. Conservation and the microbiome. Conserv Biol 2012; 26: 195 197
    [Google Scholar]
  7. Colston TJ, Jackson CR. Microbiome evolution along divergent branches of the vertebrate tree of life: what is known and unknown. Mol Ecol 2016; 25: 3776 3800
    [Google Scholar]
  8. Buhlmann KA, Akre TSB, Iverson JB, Karapatakis D, Mittermeter RA et al. A global analysis of tortoise and freshwater turtle distributions with identification of priority conservation areas. Chelonian Conserv Biol 2009; 8: 116 149
    [Google Scholar]
  9. Rhodin AGJ, Iverson JB, Bour R, Fritz U, Georges A et al. Turtles of the World: Annotated Checklist and Atlas of Taxonomy, Synonymy, Distribution, and Conservation Status. In Rhodin AGJ, Iverson JB, van Dijk PP, Saumure RA, Bhulman KA et al. (editors) Conservation Biology of Freshwater Turtles and Tortoises: A Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group CHelonian Research Monographs; 2017 p 292
    [Google Scholar]
  10. Todd BD, Willson JD, Gibbons JW, Sparling D, Bishop CA. The global status of reptiles and causes of their decline. In K S. editor Ecotoxicology of Amphibians and Reptiles Pensacola, Florida: CRC Press; 2010 pp 47 67
    [Google Scholar]
  11. Johnson AJ, Pessier AP, Wellehan JFX, Childress A, Norton TM et al. Ranavirus infection of free-ranging and captive box turtles and tortoises in the United States. J Wildl Dis 2008; 44: 851 863
    [Google Scholar]
  12. Zhang J, Finlaison DS, Frost MJ, Gestier S, Gu X et al. Identification of a novel nidovirus as a potential cause of large scale mortalities in the endangered Bellinger River snapping turtle (Myuchelys georgesi). PLoS One 2018; 13: e0205209
    [Google Scholar]
  13. De VR, Geissler K, Elmore S, Rotstein D, Dipl A et al. Ranavirus-associated morbitity and mortality in a group of captive eastern box turtles (Terrapene carolina carolina). J Zoo Wildl Med 2004; 35: 534 543
    [Google Scholar]
  14. Shreiner AB, Kao JY, Young VB. The gut microbiome in health and in disease. Curr Opin Gastroenterol 2015; 31: 69 75
    [Google Scholar]
  15. Wang BH, Yao MF, LX L, Ling ZX, LJ L. The human microbiota in health and disease. Engineering 2017; 3: 71 82
    [Google Scholar]
  16. Ford SA, King KC. Harnessing the power of defensive microbes: evolutionary implications in nature and disease control. PLoS Pathog 2016; 12: 1 12
    [Google Scholar]
  17. Bates KA, Clare FC, O’Hanlon S, Bosch J, Brookes L et al. Amphibian chytridiomycosis outbreak dynamics are linked with host skin bacterial community structure. Nat Commun 2018; 9: 1 11
    [Google Scholar]
  18. Jani AJ, Knapp RA, Briggs CJ. Epidemic and endemic pathogen dynamics correspond to distinct host population microbiomes at a landscape scale. Proc R Soc B Biol Sci 2017; 284: 20170944
    [Google Scholar]
  19. Wirth W, Schwarzkopf L, Skerratt LF, Ariel E. Ranaviruses and reptiles. PeeJ 2018; 6: e6083
    [Google Scholar]
  20. Harrison XA, Price SJ, Hopkins K, Leung WTM, Sergent C et al. Host microbiome richness predicts resistance to disturbance by pathogenic infection in a vertebrate host..
  21. Jua T, Zhao S, Knott K, Li X, Liu Y et al. The gastrointestinal tract microbiota of northern white-cheeked gibbons (Nomascus leucogenys) varies with age and captive condition. Sci Rep 2018; 16: 3214
    [Google Scholar]
  22. Becker MH, Richards-Zawacki CL, Gratwicke B, Belden LK. The effect of captivity on the cutaneous bacterial community of the critically endangered Panamanian golden frog (Atelopus zeteki). Biol Conserv 2014; 176: 199 206
    [Google Scholar]
  23. Loudon AH, Woodhams DC, Parfrey LW, Archer H, Knight R et al. Microbial community dynamics and effect of environmental microbial reservoirs on red-backed salamanders (Plethodon cinereus). Isme J 2014; 8: 830 840
    [Google Scholar]
  24. Kohl KD, Brun A, Magallanes M, Brinkerhoff J, Laspiur A et al. Gut microbial ecology of lizards: insights into diversity in the wild, effects of captivity, variation across gut regions and transmission. Mol Ecol 2017; 26: 1175 1189
    [Google Scholar]
  25. Nowakiewicz A, Majer B, Gnat S, Wójcik M, Dziedzic R et al. Aerobic bacterial microbiota isolated from the cloaca of the European pond turtle (Emys orbicularis) in Poland. J Wildl Dis 2013; 51: 255 259
    [Google Scholar]
  26. Madison JD, Austin S, Davis DR, Kerby JL. Bacterial microbiota response in Graptemys pseudogeographica to captivity and Roundup ® exposure. Copeia 2018; 106: 580 588
    [Google Scholar]
  27. Ahasan MS, Waltzek TB, Huerlimann R, Ariel E. Comparative analysis of gut bacterial communities of green turtles (Chelonia mydas) pre-hospitalization and post-rehabilitation by high-throughput sequencing of bacterial 16S rRNA gene. Microbiol Res 2018; 207: 91 99
    [Google Scholar]
  28. Ahasan MS, Waltzek TB, Huerlimann R, Ariel E. Fecal bacterial communities of wild-captured and stranded green turtles (Chelonia mydas) on the Great Barrier Reef. FEMS Microbiol Ecol 2017; 93: 1 11
    [Google Scholar]
  29. Ahasan MS, Kinobe R, Elliott L, Owens L, Scott J et al. Bacteriophage versus antibiotic therapy on gut bacterial communities of juvenile green turtle, Chelonia mydas . Environ Microbiol 2019
    [Google Scholar]
  30. Price JT, Paladino F V, Lamont MM, Witherington BE, Bates ST et al. Characterization of the juvenile green turtle (Chelonia mydas) microbiome throughout an ontogenetic shift from pelagic to neritic habitats. PLoS One 2017; 12: 1 13
    [Google Scholar]
  31. Biagi E, D’Amico F, Soverini M, Angelini V, Barone M et al. Faecal bacterial communities from Mediterranean loggerhead sea turtles (Caretta caretta). Environ Microbiol Rep 2019; 11: 361 371
    [Google Scholar]
  32. Abdelrhman KFA, Bacci G, Mancusi C, Mengoni A, Serena F et al. A first insight into the gut microbiota of the sea turtle Caretta caretta. Front Microbiol 2016; 7: 1 5
    [Google Scholar]
  33. Arizza V, Vecchioni L, Caracappa S, Sciurba G, Berlinghieri F et al. New insights into the gut microbiome in loggerhead sea turtles Caretta caretta stranded on the Mediterranean coast. PLoS One 2019; 14: e0220329
    [Google Scholar]
  34. Campos P, Guivernau M, Prenafeta-boldú FX, Cardona L. Fast acquisition of a polysaccharide fermenting gut microbiome by juvenile green turtles Chelonia mydas after settlement in coastal habitats. Microbiome 2018; 6: 69
    [Google Scholar]
  35. Sarmiento-Ramírez JM, Van Der Voort M, Raaijmakers JM, Diéguez-Uribeondo J. Unravelling the microbiome of eggs of the endangered sea turtle Eretmochelys imbricata identifies bacteria with activity against the emerging pathogen Iusarium falciforme . PLoS One 2014; 9:
    [Google Scholar]
  36. Rosado-Rodríguez G, Maldonado-Ramírez SL. Mycelial fungal diversity associated with the leatherback sea turtle (Dermochelys coriacea) nests from western Puerto Rico. Chelonian Conserv Biol 2016; 15: 265 272
    [Google Scholar]
  37. Keene EL. Microorganisms from Sand, Cloacal Fluid, and Eggs of Lepidochelys olivacea and Standard Testing of Cloacal Fluid Antimicrobial Properties Indiana University; 2012
    [Google Scholar]
  38. Sarmiento-Ramirez JM, Sim J, Van West P, Dieguez-Uribeondo J. Isolation of fungal pathogens from eggs of the endangered sea turtle species Chelonia mydas in Ascension Island. J Mar Biol Assoc United Kingdom 2017; 97: 661 667
    [Google Scholar]
  39. Al-bahry S, Mahmoud I, Elshafie A, Al-harthy A, Al-ghafri S et al. Bacterial flora and antibiotic resistance from eggs of green turtles Chelonia mydas: An indication of polluted effluents. Mar Pollut Bull 2009; 58: 720 725
    [Google Scholar]
  40. Goławska O, Zając M, Maluta A, Pristas P, Ľ H et al. Complex bacterial flora of imported PET tortoises deceased during quarantine: another zoonotic threat?. Comp Immunol Microbiol Infect Dis 2019; 65: 154 159
    [Google Scholar]
  41. Nieto‐Claudin A, Esperón F, Blake S, Deem SL. Antimicrobial resistance genes present in the faecal microbiota of free‐living Galapagos tortoises (Chelonoidis porteri). Zoonoses Public Health 2019
    [Google Scholar]
  42. García-De la Peña C, Rojas-Domínguez M, Ramírez-Bautista A, Vaca-Paniagua F, Díaz-Velásquez C et al. Oral bacterial microbiome of the Bolson tortoise Gopherus flavomarginatus at the Reserva de la Biosfera Mapimí, Mexico Cristina. Rev Mex Biodivers 2019; 90: e902683
    [Google Scholar]
  43. Gaillard DL. Population Genetics and Microbial Communities of the Gopher Tortoise (Gopherus polyphemus) University of Southern Mississippi; 2014
    [Google Scholar]
  44. Weitzman CL. Upper Respiratory Microbes in North American Tortoises (Genus Gopherus) University of Nevada: Reno; 2017
    [Google Scholar]
  45. Rene RPA. Physically effective figer threshold, apparent digestibility, and novel fecal microbiome identification of the leopard tortoisePhysically Effective Figer Threshold, Apparent Digestibility, and Novel Fecal Microbiome Identification of the Leopard Tortoise (Stigmochelys pardalis) California Polytechnic State University;
    [Google Scholar]
  46. Kopečný J, Mrázek J, Killer J. The presence of bifidobacteria in social insects, fish and reptiles. Folia Microbiol 2010; 55: 336 339
    [Google Scholar]
  47. Rawski M, Kierończyk B, Świątkiewicz S, Józefiak D. Long-term study on single and multiple species probiotic preparations for florida softshell turtle (Apalone ferox) nutrition. Anim Sci Pap Reports 2018; 36: 87 98
    [Google Scholar]
  48. Rawski M, Kieronczyk B, Dlugosz J, Swiatkiewicz S, Józefiak D. Dietary probiotics affect gastrointestinal microbiota, histological structure and shell mineralization in turtles. PLoS One 2016; 11: 1 16
    [Google Scholar]
  49. Ferronato BO, Marques TS, Souza FL, Verdade LM, Matushima ER. Oral bacterial microbiota and traumatic injuries of free-ranging Phrynops geoffroanus (Testudines, Chelidae) in southeastern Brazil. Phyllomedusa 2009; 8: 19 25
    [Google Scholar]
  50. Zancolli G, Mahsberg D, Sickel W, Keller A. Reptiles as reservoirs of bacterial infections: real threat or methodological bias?. Microb Ecol 2015; 70: 579 584
    [Google Scholar]
  51. Sardina KE. Increasing Alligator Snapping Turtle Head-Starting Success Through Enrichment and Inoculation of Hatchlings with Digestive Microbiota. Missouri State University; 2018
    [Google Scholar]
  52. Zhang X, Pneg L, Wang Y, Liang Q, Deng B et al. Effect of dietary supplementation of probiotic on performand and intestinal microflora of Chinese soft-shelled turtle (Trionyx sinensis). Aquat Nutr 2014; 20: 667 674
    [Google Scholar]
  53. de Morais BP, de Oliveria KW, Malvásio A, de Kleverson AG, Pimenta RS. Enterobacteriaceae associated with eggs of Podocnemis expansa and Podocnemis unifilis (Testudines : Chelonia) in nonpolluted sites of national Park of Araguaia Plains, Brazil. J Zoo Wildl Med 2010; 41: 656 661
    [Google Scholar]
  54. Pereira AG, Sterli J, Moreira FRR, Schrago CG. Molecular phylogenetics and evolution multilocus phylogeny and statistical biogeography clarify the evolutionary history of major lineages of turtles. Mol Phylogenet Evol 2017; 113: 59 66
    [Google Scholar]
  55. Weitzman CL, Gibb K, Christian K. Skin bacterial diversity is higher on lizards than sympatric frogs in tropical Australia. PeerJ 2018 1 15
    [Google Scholar]
  56. Allender MC, Baker S, Britton M, Kent AD. Snake fungal disease alters skin bacterial and fungal diversity in an endangered rattlesnake. Sci Rep 2018; 8: 12147
    [Google Scholar]
  57. Ross AA, Hoffmann AR, Neufeld JD. The skin microbiome of vertebrates. Microbiome 2019; 7: 79
    [Google Scholar]
  58. Lovich JE, Ennen JR, Agha M, Gibbons JW. Where have all the turtles gone, and why does it matter?. Bioscience 2018; 68: 771 781
    [Google Scholar]
  59. Iverson JB. Biomass in turtle populations: a neglected subject. Oecologia 1982; 55: 69 76
    [Google Scholar]
  60. Dash S, Das S k SJ, Thatoi HN. Epidermal mucus, a major determinant in fish health: a review. Iran J Vet Res 2018; 19: 72 81
    [Google Scholar]
  61. Ducker SC. A new species of Basicladia on Australian freshwater turtles. Hydrobiologia 1958; 10: 157 174
    [Google Scholar]
  62. Skinner S, Fitzsimmons N, Entwisle TJ. The moss-back alga (Cladophorophyceae, Chlorophyta) on two species of freshwater turtles in the Kimberleys. Telpea 2008; 12: 279 284
    [Google Scholar]
  63. Proctor VW. The growth of Basicladia on turtles. Ecology 1958; 39: 634 645
    [Google Scholar]
  64. Neil WT, Allen ER. Algae on turtles: some additional considerations. Ecology 1954; 35: 581 584
    [Google Scholar]
  65. Burgin S, Renshaw A. Algae and the Australian eastern long-necked turtle Chelodina longicollis . Am Midl Nat 2008; 160: 61 68
    [Google Scholar]
  66. Cann J, Sadlier R. Freshwater Turtles of Australia Clayton South, AU: CSIRO Publishing; 2017
    [Google Scholar]
  67. Lauer A, Simon MA, Banning JL, André E, Duncan K et al. Common cutaneous bacteria from the eastern red-backed salamander can inhibit pathogenic fungi. Copeia 2007; 2007: 630 640
    [Google Scholar]
  68. Doyle JJ, Doyle JL. A rapid procedure for DNA purification from small quantities of fresh leaf tissue. Phytochem Bull 1987; 19: 11 15
    [Google Scholar]
  69. Illumina 16S metagenomic sequencing library preparation. Illumina 2017 1 28
    [Google Scholar]
  70. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 2013; 41: 1 11
    [Google Scholar]
  71. Rohland N, Reich D. Cost-Effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Res 2012; 22: 939 946
    [Google Scholar]
  72. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 2016; 13: 581
    [Google Scholar]
  73. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 2019; 37: 852 857
    [Google Scholar]
  74. McKnight DT, Schwarzkopf L, Huerlimann R, Bower DS, Alford RA et al. microDecon: a highly accurate read‐subtraction tool for the post-sequencing removal of contamination in metabarcoding studies. Environ DNA 2019; 1: 14 25
    [Google Scholar]
  75. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 2010; 11: R106
    [Google Scholar]
  76. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-Seq data with DESeq2. Genome Biol 2014; 15: 550
    [Google Scholar]
  77. Oksanen JF, Blanchet FG, Friendly M, Kindt R, Legendre P et al. vegan: Community ecology package. https://cran.r-project.org/package=vegan . 2017
  78. McKnight DT, Huerlimann R, Bower DS, Schwarzkopf L, Alford RA et al. Methods for normalizing microbiome data: an ecological perspective. Methods Ecol Evol 2019; 10: 389 400
    [Google Scholar]
  79. Team RC R: a language and environment for statistical computing. 2017
  80. Fox J, Weisberg S. An R Companion to Applied Regression , 2nd ed. CA: Sage; 2011
    [Google Scholar]
  81. Findley K, Oh J, Yang J, Conlan S, Deming C et al. Topographic diversity of fungal and bacterial communities in human skin. Nature 2013; 498: 367 370
    [Google Scholar]
  82. Grice EA, Segre JA. The skin microbiome. Natl Rev Microbiol 2011; 9: 244 253
    [Google Scholar]
  83. Bataille A, Lee-cruz L, Tripathi B, Kim H, Waldman B. Microbiome variation across amphibian skin regions: implications for chytridiomycosis mitigation efforts. Microb Ecol 2016; 71: 221 232
    [Google Scholar]
  84. Lowrey L, Woodhams DC, Tacchi L. Topographical mapping of the rainbow trout (Oncorhynchus mykiss) microbiome reveals a diverse bacterial community with antifungal properties in the skin. Appl Environ Microbiol 2015; 81: 6915 6925
    [Google Scholar]
  85. Ward LM, Hemp J, Shih PM, McGlynn SE, Fischer WW. Evolution of phototrophy in the Chloroflexi phylum driven by horizontal gene transfer. Front Microbiol 2018; 9: 260
    [Google Scholar]
  86. Katharine Coykendall D, Cornman RS, Prouty NG, Brooke S, Demopoulos AWJ et al. Molecular characterization of Bathymodiolus mussels and gill symbionts associated with chemosynthetic habitats from the U.S. Atlantic margin. PLoS One 2019; 14: 1 28
    [Google Scholar]
  87. DeChaine EG, Cavanaugh CM. Symbioses of methanotrophs and deep-sea mussels (Mytilidae: Bathymodiolinae). Progress in Molecular and Subcellular Biology 2005 pp 227 249
    [Google Scholar]
  88. Petersen JM, Dubilier N. Methanotrophic symbioses in marine invertebrates. Environ Microbiol Rep 2009; 1: 319 335
    [Google Scholar]
  89. Ghashghavi M. Microbial Methan Oxidation in Paddy Fields Radbound University; 2019
    [Google Scholar]
  90. Mcllroy SJ, Nielsen PH. The Family Saprospiraceae. In Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F. (editors) The Prokaryotes Berlin, Heidelberg: Springer; 2014
    [Google Scholar]
  91. Komarek J. Review of the cyanobacterial genera implying planktic species after recent taxonomic revisions according to polyphasic methods: state as of 2014. Hydrobiologia 2016; 764: 259 270
    [Google Scholar]
  92. Fong P, Donohoe RM, Zedler JB. Competition with macroalgae and benthic cyanobacterial mats limits phytoplankton abundance in experimental microcosms. Mar Ecol Prog Ser 1993; 100: 97 102
    [Google Scholar]
  93. Rosenberg E, De Long EF, Lory S, Stackebrandt E, Thompson F. The prokaryotes: other major lineages of bacteria and the archaea. 2014; 2014
  94. Austin B, Austin DA. Bacterial Fish Pathogens: Diseases of Farmed and Wild Fish Chichester: Springer; 2017
    [Google Scholar]
  95. Loch TP, Faisal M. Emerging flavobacterial infections in fish: a review. J Adv Res 2015; 6: 282 300
    [Google Scholar]
  96. Thompson M. Hypothetical considerations of the biomass of chelid tortoises in the River Murray and the possible influences of predation by introduced foxes. In Lunney D, Ayers D. (editors) Herpetology in Australia: A Diverse Discipline Royal Zoological Society of New South Wales; 1993 pp 219 224
    [Google Scholar]
  97. Aguirre G, Adest GA, Recht M, Morafka DJ. Preliminary investigations of the movements, thermoregulation, population structure and diet of the Bolson tortoise (Gopherus flavomarginatus) in the Mapimí Biosphere Reserve, Durango, México. Proc Desert Tortoise Counc 1979 149 165
    [Google Scholar]
  98. Rogers VM. Dietary Ecology Including Dietary Recource Partitioning of Four Species of Chelid Turtle in a Tributary of the Fitzroy River, Central Queensland Central Queensland University; 2000
    [Google Scholar]
  99. Yuan ML, Dean SH, Longo A V, Rothermel BB, Tuberville TD et al. Kinship, inbreeding and fine-scale spatial structure influence gut microbiota in a hindgut-fermenting tortoise. Mol Ecol 2015; 24: 2521 2536
    [Google Scholar]
  100. Kersters K, De Vos P, Gillis M, Swings J, Vandamme P et al. Introduction to the Proteobacteria. In Dwokin M, Falkow S, Rosenberg E, Schleifer K, Stackebrandt E et al. (editors) The Prokaryotes New York: Springer; 2006
    [Google Scholar]
  101. Thomas François, Hehemann J-H, Rebuffet E, Czjzek M, Michel G. Environmental and gut Bacteroidetes: the food connection. Front Microbiol 2011; 2: 93 [CrossRef]
    [Google Scholar]
  102. Hong P-Y, Wheeler E, Cann IKO, Mackie RI. Phylogenetic analysis of the fecal microbial community in herbivorous land and marine iguanas of the Galápagos Islands using 16S rRNA-based pyrosequencing. ISME J 2011; 5: 1461 1470 [CrossRef]
    [Google Scholar]
  103. Wang W, Cao J, Li J-R, Yang F, Li Z et al. Comparative analysis of the gastrointestinal microbial communities of bar-headed goose (Anser indicus) in different breeding patterns by high-throughput sequencing. Microbiol Res 2016; 182: 59 67 [CrossRef] [PubMed]
    [Google Scholar]
  104. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR et al. Evolution of mammals and their gut microbes. Science 2008; 320: 1647 1651 [CrossRef]
    [Google Scholar]
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