Oligotyping reveals differences between gut microbiomes of free-ranging sympatric Namibian carnivores (Acinonyx jubatus, Canis mesomelas) on a bacterial species-like level
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic-ecollection
Document type Journal Article
PubMed
25352837
PubMed Central
PMC4196554
DOI
10.3389/fmicb.2014.00526
Knihovny.cz E-resources
- Keywords
- Namibia, bacteria, black-backed jackal (Canis mesomelas), carnivores, cheetah (Acinonyx jubatus), gut microbiome, oligotyping,
- Publication type
- Journal Article MeSH
Recent gut microbiome studies in model organisms emphasize the effects of intrinsic and extrinsic factors on the variation of the bacterial composition and its impact on the overall health status of the host. Species occurring in the same habitat might share a similar microbiome, especially if they overlap in ecological and behavioral traits. So far, the natural variation in microbiomes of free-ranging wildlife species has not been thoroughly investigated. The few existing studies exploring microbiomes through 16S rRNA gene reads clustered sequencing reads into operational taxonomic units (OTUs) based on a similarity threshold (e.g., 97%). This approach, in combination with the low resolution of target databases, generally limits the level of taxonomic assignments to the genus level. However, distinguishing natural variation of microbiomes in healthy individuals from "abnormal" microbial compositions that affect host health requires knowledge of the "normal" microbial flora at a high taxonomic resolution. This gap can now be addressed using the recently published oligotyping approach, which can resolve closely related organisms into distinct oligotypes by utilizing subtle nucleotide variation. Here, we used Illumina MiSeq to sequence amplicons generated from the V4 region of the 16S rRNA gene to investigate the gut microbiome of two free-ranging sympatric Namibian carnivore species, the cheetah (Acinonyx jubatus) and the black-backed jackal (Canis mesomelas). Bacterial phyla with proportions >0.2% were identical for both species and included Firmicutes, Fusobacteria, Bacteroidetes, Proteobacteria and Actinobacteria. At a finer taxonomic resolution, black-backed jackals exhibited 69 bacterial taxa with proportions ≥0.1%, whereas cheetahs had only 42. Finally, oligotyping revealed that shared bacterial taxa consisted of distinct oligotype profiles. Thus, in contrast to 3% OTUs, oligotyping can detect fine-scale taxonomic differences between microbiomes.
Department of Biological Sciences University of Namibia Windhoek Namibia
Evolutionary Ecology Leibniz Institute for Zoo and Wildlife Research Berlin Germany
Evolutionary Genetics Leibniz Institute for Zoo and Wildlife Research Berlin Germany
Institute of Vertebrate Biology Academy of Sciences of the Czech Republic Brno Czech Republic
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Alcaide M., Messina E., Richter M., Bargiela R., Peplies J., Huws S. A., et al. (2012). Gene sets for utilization of primary and secondary nutrition supplies in the distal gut of endangered Iberian lynx. PLoS ONE 7:e51521 10.1371/journal.pone.0051521 PubMed DOI PMC
Amato K. R. (2013). Co-evolution in context: the importance of studying gut microbiomes in wild animals. Microbiome Sci. Med. 1, 10–29 10.2478/micsm-2013-0002 DOI
Amato K. R., Yeoman C. J., Kent A., Righini N., Carbonero F., Estrada A., et al. (2013). Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J. 7, 1344–1353 10.1038/ismej.2013.16 PubMed DOI PMC
Becker A. A., Hesta M., Hollants J., Janssens G. P., Huys G. (2014). Phylogenetic analysis of faecal microbiota from captive cheetahs reveals underrepresentation of Bacteroidetes and Bifidobacteriaceae. BMC Microbiol. 14:43 10.1186/1471-2180-14-43 PubMed DOI PMC
Benson A. K., Kelly S. A., Legge R., Ma F., Low S. J., Kim J., et al. (2010). Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc. Natl. Acad. Sci. U.S.A. 107, 18933–18938 10.1073/pnas.1007028107 PubMed DOI PMC
Bercik P., Denou E., Collins J., Jackson W., Lu J., Jury J., et al. (2011). The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 141, 599–609, 609.e1–3. 10.1053/j.gastro.2011.04.052 PubMed DOI
Bergey D. H., Buchanan R. E., Gibbons N. E. (1975). Bergey's Manual of Determinative Bacteriology. Baltimore, Williams and Wilkins Co
Bermingham E. N., Young W., Kittelmann S., Kerr K. R., Swanson K. S., Roy N. C., et al. (2013). Dietary format alters fecal bacterial populations in the domestic cat (Felis catus). Microbiologyopen 2, 173–181 10.1002/mbo3.60 PubMed DOI PMC
Bolnick D. I., Snowberg L. K., Hirsch P. E., Lauber C. L., Org E., Parks B., et al. (2014). Individual diet has sex-dependent effects on vertebrate gut microbiota. Nat. Commun. 5, 1–13 10.1038/ncomms5500 PubMed DOI PMC
Bravo J. A., Forsythe P., Chew M. V., Escaravage E., Savignac H. M., Dinan T. G., et al. (2011). Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc. Natl. Acad. Sci. U.S.A. 108, 16050–16055 10.1073/pnas.1102999108 PubMed DOI PMC
Bray J. R., Curtis J. T. (1957). An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr. 27, 325 10.2307/1942268 DOI
Caporaso J. G., Bittinger K., Bushman F. D., DeSantis T. Z., Andersen G. L., Knight R. (2010a). PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266–267 10.1093/bioinformatics/btp636 PubMed DOI PMC
Caporaso J. G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F. D., Costello E. K., et al. (2010b). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 10.1038/nmeth.f.303 PubMed DOI PMC
Caporaso J. G., Lauber C. L., Walters W. A., Berg-Lyons D., Huntley J., Fierer N., et al. (2012). Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621–1624 10.1038/ismej.2012.8 PubMed DOI PMC
Caro T. M. (1994). Cheetahs of the Serengeti Plains: Group Living in an Asocial Species. Chicago: University of Chicago Press
Chalker V. J. (2005). Canine mycoplasmas. Res. Vet. Sci. 79, 1–8 10.1016/j.rvsc.2004.10.002 PubMed DOI
Coolon J. D., Jones K. L., Narayanan S., Wisely S. M. (2010). Microbial ecological response of the intestinal flora of Peromyscus maniculatus and P. leucopus to heavy metal contamination. Mol. Ecol. 19, 67–80 10.1111/j.1365-294X.2009.04485.x PubMed DOI
David L. A., Maurice C. F., Carmody R. N., Gootenberg D. B., Button J. E., Wolfe B. E., et al. (2013). Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563 10.1038/nature12820 PubMed DOI PMC
Delsuc F., Metcalf J. L., Wegener Parfrey L., Song S. J., González A., Knight R. (2014). Convergence of gut microbiomes in myrmecophagous mammals. Mol. Ecol. 23, 1301–1317 10.1111/mec.12501 PubMed DOI
Eaton T. L. (1974). The Cheetah—the Biology, Ecology, and Behavior of an Endangered Species. New York, NY: Van Nostrand Reinhold Company
Edgar R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 10.1093/bioinformatics/btq461 PubMed DOI
Edgar R. C., Haas B. J., Clemente J. C., Quince C., Knight R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 10.1093/bioinformatics/btr381 PubMed DOI PMC
Eren A. M., Borisy G. G., Huse S. M., Mark Welch J. L. (2014). Oligotyping analysis of the human oral microbiome. Proc. Natl. Acad. Sci. U.S.A. 111, E2875–E2884 10.1073/pnas.1409644111 PubMed DOI PMC
Eren A. M., Maignien L., Sul W. J., Murphy L. G., Grim S. L., Morrison H. G., et al. (2013). Oligotyping: differentiating between closely related microbial taxa using 16S rRNA gene data. Methods Ecol. Evol. 4, 1111–1119 10.1111/2041-210X.12114 PubMed DOI PMC
Eren A. M., Zozaya M., Taylor C. M., Dowd S. E., Martin D. H., Ferris M. J. (2011). Exploring the diversity of Gardnerella vaginalis in the genitourinary tract microbiota of monogamous couples through subtle nucleotide variation. PLoS ONE 6:e26732 10.1371/journal.pone.0026732 PubMed DOI PMC
Ezenwa V. O., Gerardo N. M., Inouye D. W., Medina M., Xavier J. B. (2012). Animal behavior and the microbiome. Science 338, 198–199 10.1126/science.1227412 PubMed DOI
Faith D. P. (1992). Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1–10 10.1016/0006-3207(92)91201-3 DOI
Fallani M., Young D., Scott J., Norin E., Amarri S., Adam R., et al. (2010). Intestinal microbiota of 6-week-old infants across Europe: geographic influence beyond delivery mode, breast-feeding, and antibiotics. J. Pediatr. Gastroenterol. Nutr. 51, 77–84 10.1097/MPG.0b013e3181d1b11e PubMed DOI
Famularo G., De Simone C., Pandey V., Sahu A. R., Minisola G. (2005). Probiotic lactobacilli: an innovative tool to correct the malabsorption syndrome of vegetarians? Med. Hypotheses 65, 1132–1135 10.1016/j.mehy.2004.09.030 PubMed DOI
Goldenberg M., Goldenberg F., Funk S. M., Millesi E., Henschel J. (2010). Diet composition of black-backed jackals, Canis mesomelas in the Namib desert. Folia Zool. 59, 93–101
Handl S., Dowd S. E., Garcia-Mazcorro J. F., Steiner J. M., Suchodolski J. S. (2011). Massive parallel 16S rRNA gene pyrosequencing reveals highly diverse fecal bacterial and fungal communities in healthy dogs and cats. FEMS Microbiol. Ecol. 76, 301–310 10.1111/j.1574-6941.2011.01058.x PubMed DOI
Hooper L. V., Littman D. R., Macpherson A. J. (2012). Interactions between the microbiota and the immune system. Science 336, 1268–1273 10.1126/science.1223490 PubMed DOI PMC
Jenner N., Groombridge J., Funk S. (2011). Commuting, territoriality and variation in group and territory size in a black-backed jackal population reliant on a clumped, abundant food resource in Namibia. J. Zool. 248, 231–238 10.1111/j.1469-7998.2011.00811.x DOI
Kamler J. F., Stenkewitz U., Klare U., Jacobsen N. F., Macdonald D. W. (2012). Resource partitioning among cape foxes, bat-eared foxes, and black-backed jackals in South Africa. J. Wildl. Manag. 76, 1241–1253 10.1002/jwmg.354 DOI
Kau A. L., Ahern P. P., Griffin N. W., Goodman A. L., Gordon J. I. (2011). Human nutrition, the gut microbiome and the immune system. Nature 474, 327–336 10.1038/nature10213 PubMed DOI PMC
Koch H., Schmid-Hempel P. (2011). Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc. Natl. Acad. Sci. U.S.A. 108, 19288–19292 10.1073/pnas.1110474108 PubMed DOI PMC
Kuczynski J., Lauber C. L., Walters W. A., Parfrey L. W., Clemente J. C., Gevers D., et al. (2012). Experimental and analytical tools for studying the human microbiome. Nat. Rev. Genet. 13, 47–58 10.1038/nrg3129 PubMed DOI PMC
Ley R. E., Hamady M., Lozupone C., Turnbaugh P. J., Ramey R. R., Bircher J. S., et al. (2008). Evolution of mammals and their gut microbes. Science 320, 1647–1651 10.1126/science.1155725 PubMed DOI PMC
Linnenbrink M., Wang J., Hardouin E. A., Künzel S., Metzler D., Baines J. F. (2013). The role of biogeography in shaping diversity of the intestinal microbiota in house mice. Mol. Ecol. 22, 1904–1916 10.1111/mec.12206 PubMed DOI
Lozupone C., Knight R. (2005). UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228–8235 10.1128/AEM.71.12.8228-8235.2005 PubMed DOI PMC
Lozupone C., Lladser M. E., Knights D., Stombaugh J., Knight R. (2011). UniFrac: an effective distance metric for microbial community comparison. ISME J. 5, 169–172 10.1038/ismej.2010.133 PubMed DOI PMC
Magoè T., Salzberg S. L. (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963 10.1093/bioinformatics/btr507 PubMed DOI PMC
Marker L. L., Dickman A. J., Mills M. G., Jeo R. M., Macdonald D. W. (2008). Spatial ecology of cheetahs on north-central Namibian farmlands. J. Zool. 274, 226–238 10.1111/j.1469-7998.2007.00375.x DOI
Martin M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10–12 10.14806/ej.17.1.200 DOI
McKenna P., Hoffmann C., Minkah N., Aye P. P., Lackner A., Liu Z., et al. (2008). The macaque gut microbiome in health, lentiviral infection, and chronic enterocolitis. PLoS Pathog 4:e20 10.1371/journal.ppat.0040020 PubMed DOI PMC
McLellan S. L., Newton R. J., Vandewalle J. L., Shanks O. C., Huse S. M., Eren A. M., et al. (2013). Sewage reflects the distribution of human faecal Lachnospiraceae. Environ. Microbiol. 15, 2213–2227 10.1111/1462-2920.12092 PubMed DOI PMC
McMurdie P. J., Holmes S. (2013). Package “phyloseq.” Available online at: http://bioconductor.fhcrc.org/packages/2.13/bioc/manuals/phyloseq/man/phyloseq.pdf [Accessed November 26, 2013].
Muegge B. D., Kuczynski J., Knights D., Clemente J. C., Gonzalez A., Fontana L., et al. (2011). Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332, 970–974 10.1126/science.1198719 PubMed DOI PMC
Nelson T. M., Rogers T. L., Carlini A. R., Brown M. V. (2013). Diet and phylogeny shape the gut microbiota of Antarctic seals: a comparison of wild and captive animals. Environ. Microbiol. 15, 1132–1145 10.1111/1462-2920.12022 PubMed DOI
Ochman H., Worobey M., Kuo C.-H., Ndjango J.-B. N., Peeters M., Hahn B. H., et al. (2010). Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol. 8:e1000546 10.1371/journal.pbio.1000546 PubMed DOI PMC
Phillips C. D., Phelan G., Dowd S. E., McDonough M. M., Ferguson A. W., Delton Hanson J., et al. (2012). Microbiome analysis among bats describes influences of host phylogeny, life history, physiology and geography. Mol. Ecol. 21, 2617–2627 10.1111/j.1365-294X.2012.05568.x PubMed DOI
R Core Team. (2013). R: A Language and Environment for Statistical Computing. Vienna, Austria: R foundation for statistical computing. Available online at: http://www.R-project.org
Schloissnig S., Arumugam M., Sunagawa S., Mitreva M., Tap J., Zhu A., et al. (2012). Genomic variation landscape of the human gut microbiome. Nature 493, 45–50 10.1038/nature11711 PubMed DOI PMC
Schwab C., Cristescu B., Northrup J. M., Stenhouse G. B., Gänzle M. (2011). Diet and environment shape fecal bacterial microbiota composition and enteric pathogen load of grizzly bears. PLoS ONE 6:e27905 10.1371/journal.pone.0027905 PubMed DOI PMC
Sekhon J. S. (2011). Multivariate and propensity score matching software with automated balance optimization: the matching package for R. J. Stat. Softw. 42, 1–52
Sekirov I., Russell S. L., Antunes L. C. M., Finlay B. B. (2010). Gut microbiota in health and disease. Physiol. Rev. 90, 859–904 10.1152/physrev.00045.2009 PubMed DOI
Shannon C. E., Weaver W. (1949). The Mathematical Theory of Communication. Urbana: The University of Illinois Press
Spellerberg I. F., Fedor P. J. (2003). A tribute to Claude Shannon (1916–2001) and a plea for more rigorous use of species richness, species diversity and the “Shannon–Wiener” Index. Glob. Ecol. Biogeogr. 12, 177–179 10.1046/j.1466-822X.2003.00015.x DOI
Spor A., Koren O., Ley R. (2011). Unravelling the effects of the environment and host genotype on the gut microbiome. Nat. Rev. Microbiol. 9, 279–290 10.1038/nrmicro2540 PubMed DOI
Stanier R. Y., Bazine G. C. (1977). Phototrophic prokaryotes: the cyanobacteria. Annu. Rev. Microbiol. 31, 225–274 10.1146/annurev.mi.31.100177.001301 PubMed DOI
Suchodolski J. (2011). Intestinal microbiota of dogs and cats: a bigger world than we thought. Vet. Clin. North Am. Small Anim. Pract. 41, 261–272 10.1016/j.cvsm.2010.12.006 PubMed DOI PMC
Suchodolski J. S., Dowd S. E., Westermarck E., Steiner J. M., Wolcott R. D., Spillmann T., et al. (2009). The effect of the macrolide antibiotic tylosin on microbial diversity in the canine small intestine as demonstrated by massive parallel 16S rRNA gene sequencing. BMC Microbiol. 9:210 10.1186/1471-2180-9-210 PubMed DOI PMC
Swanson K. S., Dowd S. E., Suchodolski J. S., Middelbos I. S., Vester B. M., Barry K. A., et al. (2010). Phylogenetic and gene-centric metagenomics of the canine intestinal microbiome reveals similarities with humans and mice. ISME J. 5, 639–649 10.1038/ismej.2010.162 PubMed DOI PMC
Tun H. M., Brar M. S., Khin N., Jun L., Hui R. K.-H., Dowd S. E., et al. (2012). Gene-centric metagenomics analysis of feline intestinal microbiome using 454 junior pyrosequencing. J. Microbiol. Methods 88, 369–376 10.1016/j.mimet.2012.01.001 PubMed DOI PMC
Turnbaugh P. J., Ley R. E., Mahowald M. A., Magrini V., Mardis E. R., Gordon J. I. (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1131 10.1038/nature05414 PubMed DOI
Turnbaugh P. J., Ridaura V. K., Faith J. J., Rey F. E., Knight R., Gordon J. I. (2009). The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 1, 6ra14 10.1126/scitranslmed.3000322 PubMed DOI PMC
VanderWaal K. L., Atwill E. R., Isbell L. A., McCowan B. (2013). Linking social and pathogen transmission networks using microbial genetics in giraffe (Giraffa camelopardalis). J. Anim. Ecol. 83, 406–414 10.1111/1365-2656.12137 PubMed DOI
Wachter B., Jauernig O., Breitenmoser U. (2006). Determination of prey hair in faeces of free-ranging Namibian cheetahs with a simple method. Cat. News 44, 8–9
Walton L. R., Joly D. O. (2003). Canis mesomelas. Mamm. Species 715, 1–9 10.1644/715 DOI
Waltzek T. B., Cortés-Hinojosa G., Wellehan J. F. X., Jr., Gray G. C. (2012). Marine mammal zoonoses: a review of disease manifestations. Zoonoses Public Health 59, 521–535 10.1111/j.1863-2378.2012.01492.x PubMed DOI PMC
Wang Q., Garrity G. M., Tiedje J. M., Cole J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 10.1128/AEM.00062-07 PubMed DOI PMC
Wickham H. (2009). ggplot2: Elegant Graphics for Data Analysis. New York, NY: Springer
Wu G. D., Chen J., Hoffmann C., Bittinger K., Chen Y.-Y., Keilbaugh S. A., et al. (2011). Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105–108 10.1126/science.1208344 PubMed DOI PMC
Yeoman C. J., Chia N., Yildirim S., Miller M. E. B., Kent A., Stumpf R., et al. (2011). Towards an evolutionary model of animal-associated microbiomes. Entropy 13, 570–594 10.3390/e13030570 DOI
Zhang H., Chen L. (2010). Phylogenetic analysis of 16S rRNA gene sequences reveals distal gut bacterial diversity in wild wolves (Canis lupus). Mol. Biol. Rep. 37, 4013–4022 10.1007/s11033-010-0060-z PubMed DOI