in

Anthropogenic interferences lead to gut microbiome dysbiosis in Asian elephants and may alter adaptation processes to surrounding environments

  • 1.

    Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59 (2012).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 2.

    Hooper, D. U. et al. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486, 105 (2012).

    ADS  CAS  Article  Google Scholar 

  • 3.

    Taylor-Brown, A. et al. The impact of human activities on Australian wildlife. PLoS ONE 14(1), e0206958 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 4.

    Hunter, P. The human impact on biological diversity. How species adapt to urban challenges sheds light on evolution and provides clues about conservation. EMBO Rep. 8(4), 316–318 (2007).

  • 5.

    Woinarski, J. C. Z., Burbidge, A. A. & Harrison, P. L. Ongoing unraveling of a continental fauna: Decline and extinction of Australian mammals since European settlement. Proc. Natl. Acad. Sci. 112(15), 4531 (2015).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 6.

    Cho, I. & Blaser, M. J. The human microbiome: At the interface of health and disease. Nat. Rev. Genet. 13(4), 260–270 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 7.

    Cryan, J. F. & Dinan, T. G. Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13(10), 701–712 (2012).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 8.

    Kau, A. L., Ahern, P. P., Griffin, N. W., Goodman, A. L. & Gordon, J. I. Human nutrition, the gut microbiome and the immune system. Nature 474(7351), 327–336 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 9.

    Inserra, A. et al. Mice lacking Casp 1, Ifngr and Nos2 genes exhibit altered depressive- and anxiety-like behaviour, and gut microbiome composition. Sci. Rep. 9(1), 6456 (2019).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 10.

    Kuti, D. et al. Gastrointestinal (non-systemic) antibiotic rifaximin differentially affects chronic stress-induced changes in colon microbiome and gut permeability without effect on behavior. Brain Behav. Immun. 84, 218–228 (2020).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 11.

    Bharwani, A. et al. Structural & functional consequences of chronic psychosocial stress on the microbiome & host. Psychoneuroendocrinology. 63, 217–227 (2016).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 12.

    Wasimuddin, Menke, S., Melzheimer, J., Thalwitzer, S., Heinrich, S., Wachter, B. et al. Gut microbiomes of free-ranging and captive Namibian cheetahs: Diversity, putative functions and occurrence of potential pathogens. Mol. Ecol. 26(20), 5515–5527 (2017).

  • 13.

    Sommer, F. et al. The gut microbiota modulates energy metabolism in the hibernating brown bear Ursus arctos. Cell Rep. 14(7), 1655–1661 (2016).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 14.

    Ley, R. E. et al. Evolution of mammals and their gut microbes. Science (New York, NY). 320(5883), 1647–1651 (2008).

    ADS  CAS  Article  Google Scholar 

  • 15.

    Wang, J. et al. Dietary history contributes to enterotype-like clustering and functional metagenomic content in the intestinal microbiome of wild mice. Proc. Natl. Acad. Sci. U.S.A. 111(26), E2703–E2710 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 16.

    Koch, H. & Schmid-Hempel, P. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc. Natl. Acad. Sci. U.S.A. 108(48), 19288–19292 (2011).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 17.

    Schmidt, E., Mykytczuk, N. & Schulte-Hostedde, A. I. Effects of the captive and wild environment on diversity of the gut microbiome of deer mice (Peromyscus maniculatus). ISME J. 13(5), 1293–1305 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 18.

    Lahdenperä, M., Mar, K.U., Courtiol, A., Lummaa, V. Differences in age-specific mortality between wild-caught and captive-born Asian elephants. Nat. Commun. 9(1), 3023 (2018).

  • 19.

    Sun, C. H., Liu, H. Y., Liu, B., Yuan, B. D. & Lu, C. H. Analysis of the gut microbiome of wild and captive Pere David’s deer. Front. Microbiol. 10, 2331 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  • 20.

    Ryser-Degiorgis, M.-P. Wildlife health investigations: Needs, challenges and recommendations. BMC Vet. Res. 9(1), 223 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  • 21.

    Stallknecht, D. E. Impediments to wildlife disease surveillance, research, and diagnostics. Curr. Top. Microbiol. Immunol. 315, 445–461 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 22.

    Soulsbury, C. D. et al. The welfare and ethics of research involving wild animals: A primer. Methods Ecol. Evol. 11(10), 1164–1181 (2020).

    Article  Google Scholar 

  • 23.

    Amato, K. R. et al. Using the gut microbiota as a novel tool for examining colobine primate GI health. Global Ecol. Conserv. 7, 225–237 (2016).

    Article  Google Scholar 

  • 24.

    Gehrig, J.L., Venkatesh, S., Chang, H.W., Hibberd, M.C., Kung, V.L., Cheng, J. et al. Effects of microbiota-directed foods in gnotobiotic animals and undernourished children. Science (New York, NY). 365(6449) (2019).

  • 25.

    Choudhury, A., Lahiri Choudhury, D.K., Desai, A., Duckworth, J.W., Easa, P.S., Johnsingh, A.J.T. et al. Elephas maximus. The IUCN red list of threatened species. p. e.T7140A12828813 (2008).

  • 26.

    Zhang, C., Xu, B., Lu, T. & Huang, Z. Metagenomic analysis of the fecal microbiomes of wild asian elephants reveals microflora and enzymes that mainly digest hemicellulose. J. Microbiol. Biotechnol. 29(8), 1255–1265 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 27.

    Ilmberger, N. et al. A comparative metagenome survey of the fecal microbiota of a breast- and a plant-fed Asian elephant reveals an unexpectedly high diversity of glycoside hydrolase family enzymes. PLoS ONE 9(9), e106707 (2014).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 28.

    Songer, M., Aung, M., Allendorf, T. D., Calabrese, J. M. & Leimgruber, P. Drivers of change in Myanmar’s wild elephant distribution. Trop. Conserv. Sci. 9(4), 1940082916673749 (2016).

    Article  Google Scholar 

  • 29.

    Crawley, J. A. H. et al. Investigating changes within the handling system of the largest semi-captive population of Asian elephants. PLoS ONE 14(1), e0209701 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 30.

    Oo, Z. M. Health issues of captive Asian elephants in Myanmar. Gajah. 36, 21–22 (2012).

    Google Scholar 

  • 31.

    Chel, H.M., Iwaki, T., Hmoon, M., Thaw, Y.N., Chan Soe, N., Win, S.Y., et al. Morphological and molecular identification of cyathostomine gastrointestinal nematodes of Murshidia and Quilonia species from Asian elephants in Myanmar. Int. J. Parasitol. Parasites Wildl. (2020).

  • 32.

    Sukumar, R., Santiapillai, C. Elephas maximus: Status and distribution. in The Proboscidea: Evolution and Palaeoecology of Elephants and their Relatives 327–331 (Oxford University Press, New York, 1996).

  • 33.

    Leimgruber, P. et al. Current status of Asian elephants in Myanmar. Gajah. 35, 76–86 (2011).

    Google Scholar 

  • 34.

    Prakash, T.G.S.L., Indrajith, W.A.A.D.U., Aththanayaka, A.M.C.P., Karunarathna, S., Botejue, M., Nijman, V. et al. Illegal capture and internal trade of wild Asian elephants (Elephas maximus) in Sri Lanka. Nat. Conserv. 42, 51–69 (2020).

  • 35.

    Clubb, R. & Mason, G. A Review of the Welfare of Zoo Elephants in Europe: A Report Commissioned by the RSPCA (Animal BehaviourResearch Group, University of Oxford, Oxford, 2002).

    Google Scholar 

  • 36.

    Millspaugh, J.J., Burke, T., Van Dyk, G., Slotow, R., Washburn, B.E., Woods, R.J. Stress response of working African elephants to transportation and safari adventures. J. Wildl. Manag. 1257–1260 (2007).

  • 37.

    Clubb, R. et al. Compromised survivorship in zoo elephants. Science (New York, NY). 322(5908), 1649 (2008).

    ADS  CAS  Article  Google Scholar 

  • 38.

    Easton, A.V., Quinones, M., Vujkovic-Cvijin, I., Oliveira, R.G., Kepha, S., Odiere, M.R. et al. The impact of anthelmintic treatment on human gut microbiota based on cross-sectional and pre- and postdeworming comparisons in western Kenya. mBio. 10(2) (2019).

  • 39.

    Martin, I. et al. Dynamic changes in human-gut microbiome in relation to a placebo-controlled anthelminthic trial in Indonesia. PLoS Negl. Trop. Dis. 12(8), e0006620 (2018).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 40.

    He, F. et al. Variations in gut microbiota and fecal metabolic phenotype associated with Fenbendazole and Ivermectin tablets by 16S rRNA gene sequencing and LC/MS-based metabolomics in Amur tiger. Biochem. Biophys. Res. Commun. 499(3), 447–453 (2018).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 41.

    Kunz, I. G. Z. et al. Equine fecal microbiota changes associated with anthelmintic administration. J. Equine Vet. Sci. 77, 98–106 (2019).

    PubMed  Article  PubMed Central  Google Scholar 

  • 42.

    Gagliardi, A. et al. Rebuilding the gut microbiota ecosystem. Int. J. Environ. Res. Public Health. 15(8), 1679 (2018).

    PubMed Central  Article  CAS  Google Scholar 

  • 43.

    Clayton, J. B. et al. Captivity humanizes the primate microbiome. Proc. Natl. Acad. Sci. U.S.A. 113(37), 10376–10381 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 44.

    McKenzie, V. J. et al. The effects of captivity on the mammalian gut microbiome. Integr. Comp. Biol. 57(4), 690–704 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  • 45.

    Monfort, S.L. “Mayday mayday mayday”, the millennium ark is sinking! in (Holt, W.V., Brown, J.L., Comizzoli, P. eds.) Reproductive Sciences in Animal Conservation: Progress and Prospects 15–31 (Springer, New York, 2014).

  • 46.

    Gerber, L. R. Conservation triage or injurious neglect in endangered species recovery. Proc. Natl. Acad. Sci. U.S.A. 113(13), 3563–3566 (2016).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 47.

    Haworth, S.E., White, K.S., Côté, S.D., Shafer, A.B.A. Space, time and captivity: Quantifying the factors influencing the fecal microbiome of an alpine ungulate. FEMS Microbiol. Ecol. 95(7) (2019).

  • 48.

    Gibson, K. M. et al. Gut microbiome differences between wild and captive black rhinoceros—Implications for rhino health. Sci. Rep. 9(1), 7570 (2019).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 49.

    Montonye, D. R. et al. Acclimation and institutionalization of the mouse microbiota following transportation. Front. Microbiol. 9, 1085 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 50.

    Conour, L. A., Murray, K. A. & Brown, M. J. Preparation of animals for research–issues to consider for rodents and rabbits. ILAR J. 47(4), 283–293 (2006).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 51.

    Obernier, J. A. & Baldwin, R. L. Establishing an appropriate period of acclimatization following transportation of laboratory animals. ILAR J. 47(4), 364–369 (2006).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 52.

    Mir, R. A., Kleinhenz, M. D., Coetzee, J. F., Allen, H. K. & Kudva, I. T. Fecal microbiota changes associated with dehorning and castration stress primarily affects light-weight dairy calves. PLoS ONE 14(1), e0210203 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 53.

    Abhijith, T.V., Ashokkumar, M., Dencin, R.T., George, C. Gastrointestinal parasites of Asian elephants (Elephas maximus L. 1798) in south Wayanad forest division, Kerala, India. J. Parasit. Dis. 42(3), 382–390 (2018).

  • 54.

    Bansiddhi, P., Brown, J.L., Thitaram, C., Punyapornwithaya, V., Somgird, C., Edwards, K.L. et al. Changing trends in elephant camp management in northern Thailand and implications for welfare. PeerJ. 6, e5996-e (2018).

  • 55.

    Leung, J. M. & Loke, P. N. A role for IL-22 in the relationship between intestinal helminths, gut microbiota and mucosal immunity. Int. J. Parasitol. 43(3–4), 253–257 (2013).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 56.

    Kreisinger, J., Bastien, G., Hauffe, H.C., Marchesi, J., Perkins, S.E. Interactions between multiple helminths and the gut microbiota in wild rodents. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 370(1675) (2015).

  • 57.

    Lee, S. C. et al. Helminth colonization is associated with increased diversity of the gut microbiota. PLoS Negl. Trop. Dis. 8(5), e2880 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  • 58.

    Ditgen, D. et al. Harnessing the helminth secretome for therapeutic immunomodulators. Biomed. Res. Int. 2014, 964350 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 59.

    Hewitson, J. P. et al. Proteomic analysis of secretory products from the model gastrointestinal nematode Heligmosomoides polygyrus reveals dominance of venom allergen-like (VAL) proteins. J. Proteom. 74(9), 1573–1594 (2011).

    CAS  Article  Google Scholar 

  • 60.

    Chong, R. et al. Looking like the locals—Gut microbiome changes post-release in an endangered species. Anim. Microbiome. 1(1), 8 (2019).

    Article  Google Scholar 

  • 61.

    Wienemann, T. et al. The bacterial microbiota in the ceca of Capercaillie (Tetrao urogallus) differs between wild and captive birds. Syst. Appl. Microbiol. 34(7), 542–551 (2011).

    PubMed  Article  PubMed Central  Google Scholar 

  • 62.

    Pilla, R. & Suchodolski, J. S. The role of the canine gut microbiome and metabolome in health and gastrointestinal disease. Front. Vet. Sci. 6, 498 (2019).

    PubMed  Article  PubMed Central  Google Scholar 

  • 63.

    Hemarajata, P. & Versalovic, J. Effects of probiotics on gut microbiota: Mechanisms of intestinal immunomodulation and neuromodulation. Therap. Adv. Gastroenterol. 6(1), 39–51 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 64.

    Pertoldi, C., Randi, E., Ruiz-González, A., Vergeer, P. & Ouborg, J. How can genomic tools contribute to the conservation of endangered organisms. Int. J. Genomics. 2016, 4712487 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 65.

    Roth, T. L. et al. Reduced gut microbiome diversity and metabolome differences in Rhinoceros species at risk for iron overload disorder. Front. Microbiol. 10, 2291 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  • 66.

    Youngblut, N. D. et al. Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nat. Commun. 10(1), 2200 (2019).

    ADS  PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 67.

    Tatsika, S., Karamanoli, K., Karayanni, H. & Genitsaris, S. Metagenomic characterization of bacterial communities on ready-to-eat vegetables and effects of household washing on their diversity and composition. Pathogens. 8(1), 37 (2019).

    CAS  PubMed Central  Article  Google Scholar 

  • 68.

    Allan, N., Knotts, T.A., Pesapane, R., Ramsey, J.J., Castle, S., Clifford, D. et al. Conservation implications of shifting gut microbiomes in captive-reared endangered voles intended for reintroduction into the wild. Microorganisms. 6(3) (2018).

  • 69.

    Amato, K. R. et al. The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microb. Ecol. 69(2), 434–443 (2015).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 70.

    Eid, H. M. et al. Significance of microbiota in obesity and metabolic diseases and the modulatory potential by medicinal plant and food ingredients. Front. Pharmacol. 8, 387 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 71.

    Lay, C. et al. Design and validation of 16S rRNA probes to enumerate members of the Clostridium leptum subgroup in human faecal microbiota. Environ. Microbiol. 7(7), 933–946 (2005).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 72.

    Kartzinel, T. R., Hsing, J. C., Musili, P. M., Brown, B. R. P. & Pringle, R. M. Covariation of diet and gut microbiome in African megafauna. Proc. Natl. Acad. Sci. 116(47), 23588–23593 (2019).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 73.

    Pope, P. B. et al. Metagenomics of the Svalbard reindeer rumen microbiome reveals abundance of polysaccharide utilization loci. PLoS ONE 7(6), e38571 (2012).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 74.

    Warnecke, F. et al. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450(7169), 560–565 (2007).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 75.

    Evans, N. J. et al. Characterization of novel bovine gastrointestinal tract Treponema isolates and comparison with bovine digital dermatitis treponemes. Appl. Environ. Microbiol. 77(1), 138 (2011).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 76.

    Kay, G. L. et al. Differences in the faecal microbiome in Schistosoma haematobium infected children vs. uninfected children. PLoS Negl. Trop. Dis. 9(6), 0003861 (2015).

    Article  CAS  Google Scholar 

  • 77.

    Trevelline, B. K., Fontaine, S. S., Hartup, B. K. & Kohl, K. D. Conservation biology needs a microbial renaissance: A call for the consideration of host-associated microbiota in wildlife management practices. Proc. Biol. Sci. 2019(286), 20182448 (1895).

    Google Scholar 

  • 78.

    Borody, T. J., Paramsothy, S. & Agrawal, G. Fecal microbiota transplantation: Indications, methods, evidence, and future directions. Curr. Gastroenterol. Rep. 15(8), 337 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  • 79.

    Blyton, M. D. J. et al. Faecal inoculations alter the gastrointestinal microbiome and allow dietary expansion in a wild specialist herbivore, the koala. Anim. Microbiome. 1(1), 6 (2019).

    Article  Google Scholar 

  • 80.

    Guo, W. et al. Fecal microbiota transplantation provides new insight into wildlife conservation. Glob. Ecol. Conserv. 24, e01234 (2020).

    Article  Google Scholar 

  • 81.

    Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37(8), 852–857 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 82.

    Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13(7), 581–583 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 83.

    Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 26(1), 32–46 (2001).

    Google Scholar 

  • 84.

    Vazquez-Baeza, Y., Pirrung, M., Gonzalez, A. & Knight, R. EMPeror: A tool for visualizing high-throughput microbial community data. GigaScience. 2(1), 16 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  • 85.

    Bokulich, N. A. et al. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome. 6(1), 90 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 86.

    Morton, J. T. et al. Balance trees reveal microbial niche differentiation. mSystems 2(1), e00162-00166 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 87.

    Mandal, S. et al. Analysis of composition of microbiomes: A novel method for studying microbial composition. Microb. Ecol. Health Dis. 26, 27663 (2015).

    PubMed  PubMed Central  Google Scholar 


  • Source: Ecology - nature.com

    Atmospheric dynamic constraints on Tibetan Plateau freshwater under Paris climate targets

    A pilot study of eDNA metabarcoding to estimate plant biodiversity by an alpine glacier core (Adamello glacier, North Italy)