Taxonomy, not locality, influences the cloacal microbiota of two nearctic colubrids: a preliminary analysis.
Animals
Animals, Wild
/ microbiology
Bacteroidetes
/ genetics
Cloaca
/ microbiology
Colubridae
/ microbiology
DNA, Ribosomal
/ genetics
Firmicutes
/ genetics
Gastrointestinal Microbiome
/ genetics
Genetic Variation
High-Throughput Nucleotide Sequencing
/ methods
Pennsylvania
Phylogeny
Ponds
Proteobacteria
/ genetics
Tenericutes
/ genetics
Cloacal microbiota
Eastern Gartersnake
Habitat
Northern Watersnake
Tenericutes
Journal
Molecular biology reports
ISSN: 1573-4978
Titre abrégé: Mol Biol Rep
Pays: Netherlands
ID NLM: 0403234
Informations de publication
Date de publication:
Sep 2021
Sep 2021
Historique:
received:
22
05
2021
accepted:
11
08
2021
pubmed:
18
8
2021
medline:
29
1
2022
entrez:
17
8
2021
Statut:
ppublish
Résumé
The gut microbiota is an emerging frontier in wildlife research and its importance to vertebrate health and physiology is becoming ever more apparent. Reptiles, in particular snakes, have not received the same attention given to other vertebrates and the composition of their wild gut microbiome remains understudied. The primary goal of this work was to describe the cloacal microbiota of two Colubrids, the Eastern Gartersnake (Thamnophis sirtalis sirtalis) and the Northern Watersnake (Nerodia sipedon sipedon), and if their cloacal microbiota differed as well as if it did between a wetland and upland population of the former species. We utilized next-generation sequencing of cloacal swabs-a non-destructive proxy for the gut microbiota. The cloacal microbiome of Eastern Gartersnakes (N = 9) was like those of other snakes being comprised of Proteobacteria, Bacteroidetes, and Firmicutes, while that of Northern Watersnakes (N = 6) was dominated by Tenericutes. Seven microbial operational taxonomic units (OTUs), all members of Proteobacteria, were shared among all individuals and were indicative of a core microbiome in Eastern Gartersnakes, but these OTUs were not particularly relevant to Northern Watersnakes. The latter had greater OTU richness than did Eastern Gartersnakes, and habitat did not have any apparent effect on the microbial community composition in Eastern Gartersnakes. Our findings suggest host taxonomy to be a determining factor in the cloacal microbiota of snakes and that Tenericutes are associated with aquatic habitats. This is the first report to examine the cloacal microbiome of these species and provides a useful foundation for future work to build upon.
Sections du résumé
BACKGROUND
BACKGROUND
The gut microbiota is an emerging frontier in wildlife research and its importance to vertebrate health and physiology is becoming ever more apparent. Reptiles, in particular snakes, have not received the same attention given to other vertebrates and the composition of their wild gut microbiome remains understudied. The primary goal of this work was to describe the cloacal microbiota of two Colubrids, the Eastern Gartersnake (Thamnophis sirtalis sirtalis) and the Northern Watersnake (Nerodia sipedon sipedon), and if their cloacal microbiota differed as well as if it did between a wetland and upland population of the former species.
METHODS AND RESULTS
RESULTS
We utilized next-generation sequencing of cloacal swabs-a non-destructive proxy for the gut microbiota. The cloacal microbiome of Eastern Gartersnakes (N = 9) was like those of other snakes being comprised of Proteobacteria, Bacteroidetes, and Firmicutes, while that of Northern Watersnakes (N = 6) was dominated by Tenericutes. Seven microbial operational taxonomic units (OTUs), all members of Proteobacteria, were shared among all individuals and were indicative of a core microbiome in Eastern Gartersnakes, but these OTUs were not particularly relevant to Northern Watersnakes. The latter had greater OTU richness than did Eastern Gartersnakes, and habitat did not have any apparent effect on the microbial community composition in Eastern Gartersnakes.
CONCLUSIONS
CONCLUSIONS
Our findings suggest host taxonomy to be a determining factor in the cloacal microbiota of snakes and that Tenericutes are associated with aquatic habitats. This is the first report to examine the cloacal microbiome of these species and provides a useful foundation for future work to build upon.
Identifiants
pubmed: 34403035
doi: 10.1007/s11033-021-06645-x
pii: 10.1007/s11033-021-06645-x
doi:
Substances chimiques
DNA, Ribosomal
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6435-6442Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Nature B.V.
Références
McFall-Ngai M, Hadfield MG, Bosch TCG et al (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci 110:3229–3236
pubmed: 23391737
pmcid: 3587249
doi: 10.1073/pnas.1218525110
Macke E, Tasiemski A, Massol F, Callens M, Decaestecker E (2017) Life history and eco-evolutionary dynamics in light of the gut microbiota. Oikos 126:508–531
doi: 10.1111/oik.03900
West AG, Waite DW, Deines P et al (2019) The microbiome in threatened species conservation. Biol Cons 229:85–98
doi: 10.1016/j.biocon.2018.11.016
Colston TJ, Jackson CR (2016) Microbiome evolution along divergent branches of the vertebrate tree of life: what is known and unknown. Mol Ecol 25:3776–3800
pubmed: 27297628
doi: 10.1111/mec.13730
Kohl KD, Brun A, Magallanes M et al (2017) Gut microbial ecology of lizards: insights into diversity in the wild, effects of captivity, variation across gut regions and transmission. Mol Ecol 26:1175–1189
pubmed: 27862531
doi: 10.1111/mec.13921
Ren T, Kahrl AF, Wu M, Cox RM (2016) Does adaptive radiation of a host lineage promote ecological diversity of its bacterial communities? A test using gut microbiota of Anolis lizards. Mol Ecol 25:4793–4804
pubmed: 27497270
doi: 10.1111/mec.13796
Jiang HY, Ma JE, Li J et al (2017) Diets alter the gut microbiome of crocodile lizards. Front Microbiol 8:2073
pubmed: 29118742
pmcid: 5660983
doi: 10.3389/fmicb.2017.02073
Yuan ML, Dean SH, Longo AV, Rothermel BB, Tuberville TD, Zamudio KR (2015) Kinship, inbreeding and fine-scale spatial structure influence gut microbiota in a hindgut-fermenting tortoise. Mol Ecol 24:2521–2536
pubmed: 25809385
doi: 10.1111/mec.13169
Keenan SW, Engel AS, Elsey RM (2013) The alligator gut microbiome and implications for archosaur symbioses. Sci Rep 3:2877
pubmed: 24096888
pmcid: 3791443
doi: 10.1038/srep02877
Hill JG III, Hanning I, Beaupre SJ, Ricke SC, Slavik MM (2008) Denaturing gradient gel electrophoresis for the determination of bacterial species diversity in the gastrointestinal tracts of two Crotaline snakes. Herpetol Rev 39:433–438
McLaughlin RW, Cochran PA, Dowd SE (2015) Metagenomic analysis of the gut microbiota of the Timber Rattlesnake, Crotalus horridus. Mol Biol Rep 42:1187–1195
pubmed: 25663091
doi: 10.1007/s11033-015-3854-1
Colston TJ, Noonan BP, Jackson CR (2015) Phylogenetic analysis of bacterial communities in different regions of the gastrointestinal tract of Agkistrodon piscivorus, the cottonmouth snake. PLoS ONE 10:e0128793
pubmed: 26039313
pmcid: 4454441
doi: 10.1371/journal.pone.0128793
Zhang B, Ren J, Yang D, Liu S, Gong X (2018) Comparative analysis and characterization of the gut microbiota of four farmed snakes from southern China. PeerJ 7:e6658
doi: 10.7717/peerj.6658
Tang W, Zhu G, Shi Q et al (2019) Characterizing the microbiota in gastrointestinal tract segments of Rhabdophis subminiatus: dynamic changes and functional predictions. MicrobiologyOpen 8:e789. https://doi.org/10.1002/mbo3.789
Ley RE, Hamady M, Lozupone C et al (2008) Evolution of mammals and their gut microbes. Science 320:1647–1651
pubmed: 2649005
pmcid: 2649005
doi: 10.1126/science.1155725
Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6:776–788
pubmed: 18794915
pmcid: 2664199
doi: 10.1038/nrmicro1978
Hale VL, Tan CL, Niu K et al (2018) Diet versus phylogeny: a comparison of gut microbiota in captive colobine monkey species. Microb Ecol 75:515–527
pubmed: 28735426
doi: 10.1007/s00248-017-1041-8
Youngblut ND, Reischer GH, Walters W et al (2018) Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nat Commun 10:1–15. https://doi.org/10.1101/484006
Barelli C, Albanese D, Donati C et al (2015) Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: implications for conservation. Sci Rep 5:14862
pubmed: 26445280
pmcid: 4595646
doi: 10.1038/srep14862
Amato KR, Yeoman CJ, Kent A et al (2013) Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J 7:1344–1353
pubmed: 23486247
pmcid: 3695285
doi: 10.1038/ismej.2013.16
Huang BH, Chang CW, Huang CW, Gao J, Liao PC (2017) Composition and functional specialists of the gut microbiota of frogs reflect habitat differences and agricultural activity. Front Microbiol 8:2670
pubmed: 29375532
doi: 10.3389/fmicb.2017.02670
pmcid: 29375532
Sun B, Wang X, Bernstein S et al (2016) Marked variation between winter and spring gut microbiota in free-ranging Tibetan Macaques (Macaca thibetana). Sci Rep 6:26035
pubmed: 27180722
pmcid: 4867428
doi: 10.1038/srep26035
Hulse AC, McCoy CJ, Censky EJ (2001) Amphibians and reptiles of Pennsylvania and the Northeast. Comstock Publishing Associates, Ithica
Greenhalgh K, Meyer KM, Aagaard KM, Wilmes P (2016) The human gut microbiome in health: establishment and resilience of microbiota over a lifetime. Environ Microbiol 18:2103–2116
pubmed: 27059297
pmcid: 7387106
doi: 10.1111/1462-2920.13318
Videvall E, Song SJ, Bensch HM et al (2019) The development of gut microbiota in ostriches and its association with juvenile growth. Mol Ecol 2019:2653–2667
doi: 10.1111/mec.15087
Zeglin LH, Wang B, Waythomas C, Rainey F, Talbot SL (2016) Organic matter quantity and source affects microbial community structure and function following volcanic eruption on Kasatochi Island, Alaska. Environ Microbiol 18:146–158
pubmed: 26032670
doi: 10.1111/1462-2920.12924
Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
pubmed: 20383131
pmcid: 20383131
doi: 10.1038/nmeth.f.303
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
pubmed: 17586664
pmcid: 1950982
doi: 10.1128/AEM.00062-07
Risely A (2020) Applying the core microbiome to understand host-microbe systems. J Anim Ecol 89:1549–1558
Oksanen J, Blanchet FG, Kindt R et al (2013) vegan: Community Ecology Package. R package version 2.5-7. https://CRAN.R-project.org/package=vegan
R Core Development Team (2019) R: a language and environment for statistical computing. https://cran.r-project.org/
Junior F, Rui S, Siqueira AK et al (2009) Comparison of wildlife and captivity rattlesnakes (Crotalus durissus terrificus) microbiota. Pesquisa Veterinária Brasileira 29:999–1003
doi: 10.1590/S0100-736X2009001200008
Costello EK, Gordon JI, Secor SM, Knight R (2010) Postprandial remodeling of the gut microbiota in Burmese pythons. ISME J 4:1375–1385
pubmed: 20520652
doi: 10.1038/ismej.2010.71
Jho YS, Park DH, Lee JH, Cha SY, Han JS (2011) Identification of bacteria from the oral cavity and cloaca of snakes imported from Vietnam. Lab Anim Res 27:213–217
pubmed: 21998610
pmcid: 3188728
doi: 10.5625/lar.2011.27.3.213
Coyte KZ, Rakoff-Nahoum S (2019) Understanding competition and cooperation within the mammalian gut microbiome. Curr Biol 29:R538–R544
pubmed: 31163167
pmcid: 6935513
doi: 10.1016/j.cub.2019.04.017
Razin S, Yogev D, Naot Y (1998) Molecular biology and pathogenicity of mycoplasmas. Microbiol Mol Biol Rev 62:1094–1156
pubmed: 9841667
pmcid: 98941
doi: 10.1128/MMBR.62.4.1094-1156.1998
Brown DR (2002) Mycoplasmosis and immunity of fish and reptiles. Front Biosci 7:1338–1346
doi: 10.2741/brown
Palmer JL, Blake S, Wellehan JF Jr, Childress AL, Deem SL (2016) Clinical Mycoplasma sp. infections in free-living three-toed box turtles (Terrapene carolina triunguis) in Missouri, USA. J Wildl Dis 52:378–382
pubmed: 27124328
doi: 10.7589/2015-07-189
Ossiboff RJ, Raphael BL, Ammazzalorso AD et al (2015) A Mycoplasma species of Emydidae turtles in the northeastern USA. J Wildl Dis 51:466–470
pubmed: 25574806
doi: 10.7589/2014-04-086
Bano N, DeRae SA, Bennett W, Vasquez L, Hollibaugh JT (2007) Dominance of Mycoplasma in the guts of the Long-Jawed Mudsucker, Gillichthys mirabilis, from five California salt marshes. Environ Microbiol 9:2636–2641
pubmed: 17803786
doi: 10.1111/j.1462-2920.2007.01381.x
Llewellyn MS, McGinnity P, Dionne M et al (2016) The biogeography of the atlantic salmon (Salmo salar) gut microbiome. ISME J 10:1280–1284
pubmed: 26517698
doi: 10.1038/ismej.2015.189
Gross R, Guzman CA, Sebaihia M et al (2008) The missing link: Bordetella petrii is endowed with both the metabolic versatility of environmental bacteria and virulence traits of pathogenic Bordetellae. BMC Genomics 9:449
pubmed: 18826580
pmcid: 2572626
doi: 10.1186/1471-2164-9-449
Wu Y, Yang Y, Cao L et al (2018) Habitat environments impacted the gut microbiome of long-distance migratory swan geese but central species conserved. Sci Rep 8:13314
pubmed: 30190564
pmcid: 6127342
doi: 10.1038/s41598-018-31731-9
Videvall E, Strandh M, Engelbrecht A, Cloete S, Cornwallis CK (2017) Direct PCR offers a fast and reliable alternative to conventional DNA isolation methods for gut microbiomes. MSystems 2:e00132-e1117
pubmed: 29181448
pmcid: 5698494
doi: 10.1128/mSystems.00132-17
Hale VL, Tan CL, Niu K et al (2016) Effects of field conditions on fecal microbiota. J Microbiol Methods 130:180–188
pubmed: 27686380
doi: 10.1016/j.mimet.2016.09.017
Choo JM, Leong LE, Rogers GB (2015) Sample storage conditions significantly influence faecal microbiome profiles. Sci Rep 5:16350
pubmed: 26572876
pmcid: 4648095
doi: 10.1038/srep16350
Videvall E, Strandh M, Engelbrecht A, Cloete S, Cornwallis CK (2018) Measuring the gut microbiome in birds: comparison of faecal and cloacal sampling. Mol Ecol Resour 18:424–434
pubmed: 29205893
doi: 10.1111/1755-0998.12744
Zhang Y, Simon SE, Johnson JA, Allen MS (2017) Spatial microbial composition along the gastrointestinal tract of captive Attwater’s prairie chicken. Microb Ecol 73:966–977
pubmed: 27752719
doi: 10.1007/s00248-016-0870-1
Berlow M, Kohl KD, Derryberry EP (2020) Evaluation of non‐lethal gut microbiome sampling methods in a passerine bird. Ibis 162:911–923
Artavia-León A, Romero-Guerrero A, Sancho-Blanco C, Rojas N, Umaña-Castro R (2017) Diversity of aerobic bacteria isolated from oral and cloacal cavities from free-living snakes species in Costa Rica rainforest. Int Sch Res Not 2017:1–9