Southern Tamanduas (Tamandua tetradactyla) belong to the specialized placental myrmecophages. There is not much information about their intestinal microbiome. Moreover, due to their food specialization, it is difficult to create an adequate diet under breeding conditions. Therefore, we used 16S rDNA amplicon sequencing to analyze the fecal microbiome of captive Southern Tamanduas from four locations in the Czech Republic and evaluated the impact of the incoming diet and facility conditions on microbiome composition. Together with the microbiome analysis, we also quantified and identified cultivable commensals. The anteater fecal microbiome was dominated by the phyla Bacillota and Bacteroidota, while Pseudomonadota, Spirochaetota, and Actinobacteriota were less abundant. At the taxonomic family level, Lachnospiraceae, Prevotellaceae, Bacteroidaceae, Oscillospiraceae, Erysipelotrichaceae, Spirochaetaceae, Ruminococcaceae, Leuconostocaceae, and Streptococcaceae were mainly represented in the fecal microbiome of animals from all locations. Interestingly, Lactobacillaceae dominated in the location with a zoo-made diet. These animals also had significantly lower diversity of gut microbiome in comparison with animals from other locations fed mainly with a complete commercial diet. Moreover, captive conditions of analyzed anteater included other factors such as the enrichment of the diet with insect-based products, probiotic interventions, the presence of other animals in the exposure, which can potentially affect the composition of the microbiome and cultivable microbes. In total, 63 bacterial species from beneficial commensal to opportunistic pathogen were isolated and identified using MALDI-TOF MS in the set of more than one thousand selected isolates. Half of the detected species were present in the fecal microbiota of most animals, the rest varied across animals and locations.

Department of Ethology and Companion Animal Science Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Kamycka 129 165 00 Prague 6 Czech Republic

Department of Microbiology Nutrition and Dietetics Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamycka 129 165 00 Prague 6 Czech Republic

Institute of Animal Physiology and Genetics The Czech Academy of Sciences v v i Videnska 1083 142 20 Prague Czech Republic

Zobrazit více v PubMed

IUCN 2023. The IUCN Red List of Threatened Species. Version 2022-2. ISSN 2307-8235 https://www.iucnredlist.org

Delsuc F, et al. Convergence of gut microbiomes in myrmecophagous mammals. Mol Ecol. 2014;23(6):1301–1317. doi: 10.1111/mec.12501. PubMed DOI

Firmino MD, et al. External and digestive system morphology of the Tamandua tetradactyla. Anat Histol Embryol. 2020;49(1):97–104. doi: 10.1111/ahe.12494. PubMed DOI

Gull JM, et al. Digestive physiology of captive giant anteaters (Myrmecophaga tridactyla): determinants of faecal dry matter content. J Anim Physiol Anim Nutr. 2015;99(3):565–576. doi: 10.1111/jpn.12223. PubMed DOI

Teullet S, et al. Metagenomics uncovers dietary adaptations for chitin digestion in the gut microbiota of convergent myrmecophagous mammals. bioRxiv. 2023;2023.04.21.537829. PubMed PMC

Gaudin TJ, Hicks P, Di Blanco Y. Myrmecophaga tridactyla (Pilosa: Myrmecophagidae) Mamm Species. 2018;50(956):1–13. doi: 10.1093/mspecies/sey001. DOI

Kreutz K, Fischer F, Linsenmair KE. Timber plantations as favourite habitat for giant anteaters. Mammalia. 2012;76(2):137–142. doi: 10.1515/mammalia-2011-0049. DOI

Muegge BD, et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science. 2011;332(6032):970–974. doi: 10.1126/science.1198719. PubMed DOI PMC

Clark A, et al. Survey of feeding practices, body condition and faeces consistency in captive ant-eating mammals in the UK. J Zoo Aquar Res. 2016;4(4):183–195.

McKenzie VJ, et al. The effects of captivity on the mammalian gut microbiome. Integr Compar Biol. 2017;57(4):690–704. doi: 10.1093/icb/icx090. PubMed DOI PMC

Sherrill-Mix S, et al. Allometry and ecology of the bilaterian gut microbiome. MBIO 2018;9(2). PubMed PMC

de Jonge N, et al., The gut microbiome of 54 mammalian species. Front. Microbiol. 2022;13. PubMed PMC

Cheng S-C, et al. Hologenomic insights into mammalian adaptations to myrmecophagy. Natl Sci Rev. 2022;10(4). PubMed PMC

Caporaso JG, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA. 2011;108(SUPPL. 1):4516–4522. doi: 10.1073/pnas.1000080107. PubMed DOI PMC

Milani C, et al. Assessing the fecal microbiota: an optimized ion torrent 16S rRNA gene-based analysis protocol. PLoS ONE. 2013;8(7). PubMed PMC

Mekadim C, et al. Dysbiosis of skin microbiome and gut microbiome in melanoma progression. BMC Microbiol. 2022;22(1). PubMed PMC

Bolyen E, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37(8):852–857. doi: 10.1038/s41587-019-0209-9. PubMed DOI PMC

Callahan BJ, et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–583. doi: 10.1038/nmeth.3869. PubMed DOI PMC

Katoh K, et al. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30(14):3059–3066. doi: 10.1093/nar/gkf436. PubMed DOI PMC

Price MN, Dehal PS, Arkin AP. FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE. 2010;5(3):e9490. doi: 10.1371/journal.pone.0009490. PubMed DOI PMC

Segata N et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12(6). PubMed PMC

Modrackova N, et al. The bifidobacterial distribution in the microbiome of captive primates reflects parvorder and feed specialization of the host. Sci Rep. 2021;11(1):15273. doi: 10.1038/s41598-021-94824-y. PubMed DOI PMC

Hungate RE, Macy J. The roll-tube method for cultivation of strict anaerobes. Bull Ecol Res Comm. 1973;17:123–126.

Modrackova N, et al. The bifidobacterial distribution in the microbiome of captive primates reflects parvorder and feed specialization of the host. Sci Rep. 2021;11(1):1–13. doi: 10.1038/s41598-021-94824-y. PubMed DOI PMC

Zoelzer F, Burger AL, Dierkes PW. Unraveling differences in fecal microbiota stability in mammals: from high variable carnivores and consistently stable herbivores. Animal Microbiome. 2021;3(1):77. doi: 10.1186/s42523-021-00141-0. PubMed DOI PMC

Yin XC, et al. Dietary perturbations alter the ecological significance of ingested Lactobacillus plantarum in the digestive tract. Sci Rep. 2017;7. PubMed PMC

Martino ME, et al. Bacterial adaptation to the host's diet is a key evolutionary force shaping drosophila-lactobacillus LESymbiosis. Cell Host Microbe. 2018;24(1):109. doi: 10.1016/j.chom.2018.06.001. PubMed DOI PMC

Ley RE, et al. Evolution of mammals and their gut microbes. Science. 2008;320(5883):1647–1651. doi: 10.1126/science.1155725. PubMed DOI PMC

Alberdi A, Martin Bideguren G, Aizpurua O. Diversity and compositional changes in the gut microbiota of wild and captive vertebrates: a meta-analysis. Sci Rep. 2021;11(1):22660. doi: 10.1038/s41598-021-02015-6. PubMed DOI PMC

Odonnell MM, et al. Core fecal microbiota of domesticated herbivorous ruminant, hindgut fermenters, and monogastric animals. MicrobiologyOpen. 2017;6(5):e00509. doi: 10.1002/mbo3.509. PubMed DOI PMC

Youngblut ND, et al. Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nat Commun. 2019;10(1):2200. doi: 10.1038/s41467-019-10191-3. PubMed DOI PMC

Amato KR, et al. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J. 2013;7(7):1344–1353. doi: 10.1038/ismej.2013.16. PubMed DOI PMC

David LA, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559. doi: 10.1038/nature12820. PubMed DOI PMC

Liu Y, Wang J, Wu C, Modulation of gut microbiota and immune system by probiotics, pre-biotics, and post-biotics. Front Nutr 2022;8. PubMed PMC

Li C, et al. Probiotics, prebiotics, and synbiotics regulate the intestinal microbiota differentially and restore the relative abundance of specific gut microorganisms. J Dairy Sci. 2020;103(7):5816–5829. doi: 10.3168/jds.2019-18003. PubMed DOI

Chapman CMC, Gibson GR, Rowland I. In vitro evaluation of single- and multi-strain probiotics: inter-species inhibition between probiotic strains, and inhibition of pathogens. Anaerobe. 2012;18(4):405–413. doi: 10.1016/j.anaerobe.2012.05.004. PubMed DOI

Neuzil-Bunesova V, et al. Feed insects as a reservoir of granadaene-producing lactococci. Front Microbiol. 2022;13. PubMed PMC

Song SJ et al. Cohabiting family members share microbiota with one another and with their dogs. eLife. 2013;2013(2). PubMed PMC

Hauffe HC, Barelli C. Conserve the germs: the gut microbiota and adaptive potential. Conserv Genet. 2019;20(1):19–27. doi: 10.1007/s10592-019-01150-y. DOI

Redford KH, et al. Conservation and the microbiome. Conserv Biol. 2012;26(2):195–197. doi: 10.1111/j.1523-1739.2012.01829.x. PubMed DOI PMC

Kohl KD, Skopec MM, Dearing MD, Captivity results in disparate loss of gut microbial diversity in closely related hosts. Conserv Physiol. 2014;2(1). PubMed PMC

Bahrndorff S, et al. The microbiome of animals: implications for conservation biology. Int J Genomics. 2016;2016:5304028. doi: 10.1155/2016/5304028. PubMed DOI PMC

Gibson KM, et al. Gut microbiome differences between wild and captive black rhinoceros—implications for rhino health. Sci Rep. 2019;9(1):7570. doi: 10.1038/s41598-019-43875-3. PubMed DOI PMC

Martiny AC. High proportions of bacteria are culturable across major biomes. ISME J. 2019;13(8):2125–2128. doi: 10.1038/s41396-019-0410-3. PubMed DOI PMC

Willem MdV, et al. Gut microbiome and health: mechanistic insights. Gut. 2022;71(5):1020. doi: 10.1136/gutjnl-2021-326789. PubMed DOI PMC

Makovska M, et al. Species and strain variability among sarcina isolates from diverse mammalian hosts. Animals. 2023;13(9). PubMed PMC

Neuzil-Bunesova V, et al. Bifidobacterium canis sp. Nov., a novel member of the bifidobacterium pseudolongum phylogenetic group isolated from faeces of a dog (Canis Lupus f. familiaris) Int J Syst Evolut Microbiol. 2020;70(9):5040–5047. doi: 10.1099/ijsem.0.004378. PubMed DOI

Bagge E, Persson M, Johansson KE. Diversity of spore-forming bacteria in cattle manure, slaughterhouse waste and samples from biogas plants. J Appl Microbiol. 2010;109(5):1549–1565. PubMed

Moore RJ, Lacey JA. Genomics of the pathogenic clostridia. Microbiol Spectrum. 2019;7(3). PubMed PMC

Guo P, et al. Clostridium species as probiotics: potentials and challenges. J Anim Sci Biotechnol. 2020;11(1). PubMed PMC

Rodriguez CI, Martiny JBH. Evolutionary relationships among bifidobacteria and their hosts and environments. BMC Genomics. 2020;21(1). PubMed PMC

Lugli GA, et al. Phylogenetic classification of six novel species belonging to the genus Bifidobacterium comprising Bifidobacterium anseris sp. nov., Bifidobacterium criceti sp. nov., Bifidobacterium imperatoris sp. nov., Bifidobacterium italicum sp. nov., Bifidobacterium margollesii sp. nov. and Bifidobacterium parmae sp. nov. Syst Appl Microbiol. 2018;41(3):173–83. PubMed

Lugli GA, et al. Exploring the biodiversity of Bifidobacterium asteroides among honey bee microbiomes. Environ Microbiol. 2022;24(12):5666–5679. doi: 10.1111/1462-2920.16223. PubMed DOI PMC

Meyer D, Stasse-Wolthuis M. The bifidogenic effect of inulin and oligofructose and its consequences for gut health. Eur J Clin Nutr. 2009;63(11):1277–1289. doi: 10.1038/ejcn.2009.64. PubMed DOI

Modrackova N, et al. Prebiotic potential of natural gums and starch for bifidobacteria of variable origins. Bioact Carbohydr Dietary Fibre. 2019;20.

Dempsey E, Corr SC. Lactobacillus spp. for gastrointestinal health: Current and future perspectives. Front Immunol. 2022;13:840245. doi: 10.3389/fimmu.2022.840245. PubMed DOI PMC

Shan C, et al. Pediococcus pentosaceus enhances host resistance against pathogen by increasing IL-1β production: understanding probiotic effectiveness and administration duration. Front. Immunol. 2021;12. PubMed PMC

Wanna W, et al. Evaluation of probiotic characteristics and whole genome analysis of Pediococcus pentosaceus MR001 for use as probiotic bacteria in shrimp aquaculture. Sci. Rep. 2021;11(1). PubMed PMC

Wang H, et al. Effects of compound probiotics on growth performance, rumen fermentation, blood parameters, and health status of neonatal Holstein calves. J Dairy Sci. 2022;105(3):2190–2200. doi: 10.3168/jds.2021-20721. PubMed DOI

Li H, et al. Pediococcus pentosaceus im96 exerts protective effects against enterohemorrhagic escherichia coli o157:H7 infection in vivo. Foods. 2021;10(12). PubMed PMC

Chen P, et al. Characterization of Streptococcus lutetiensis isolated from clinical mastitis of dairy cows. J Dairy Sci. 2021;104(1):702–714. doi: 10.3168/jds.2020-18347. PubMed DOI

Jans C, Boleij A. The road to infection: host-microbe interactions defining the pathogenicity of Streptococcus bovis/Streptococcus equinus complex members. Front Microbiol. 2018;9(APR). PubMed PMC

Wang X, et al. Antimicrobial resistance of Escherichia coli, Enterobacter spp., Klebsiella pneumoniae and Enterococcus spp. isolated from the feces of giant panda. BMC Microbiol. 2022;22(1):102. doi: 10.1186/s12866-022-02514-0. PubMed DOI PMC

Modrackova N, et al. Microbial shifts of faecal microbiota using enteral nutrition in vitro. J Funct Foods. 2021;77:104330. doi: 10.1016/j.jff.2020.104330. DOI

Bunesova V, et al. Effect of rearing systems and diets composition on the survival of probiotic bifidobacteria in the digestive tract of calves. Livest Sci. 2015;178:317–321. doi: 10.1016/j.livsci.2015.06.017. DOI

Ma J-E et al. The fecal metagenomics of malayan pangolins identifies an extensive adaptation to myrmecophagy. Front Microbiol. 2018;9. PubMed PMC

Metabolic diversity and responses of anteater clostridial isolates to chitin-based substrates