AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Avian Research Article
PDF (2.9 MB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research | Open Access

The gut microbiome and metabolome of Himalayan Griffons (Gyps himalayensis): insights into the adaptation to carrion-feeding habits in avian scavengers

Wen Wang1 ( ), Xiaolong Gao2, Sisi Zheng1, Zhuoma Lancuo3, Ying Li1, Lilin Zhu4, Jianping Hou5, Jiayi Hai5, Xin Long5, Hanxi Chen5, Alexey Druzyaka6, Kirill Sharshov7 ( )
State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xi'ning, 810016, China
College of Agriculture and Animal Husbandry, Qinghai University, Xi'ning, 810016, China
College of Finance and Economics, Qinghai University, Xi'ning, 810016, China
Xining Wild Animal Epidemic Disease Monitoring Station, Xi'ning, 810001, China
College of Eco-Environmental Engineering, Qinghai University, Xi'ning, 810016, China
Institute of Systematics and Ecology of Animals, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, 630091, Russia
Federal Research Center of Fundamental and Translational Medicine, Novosibirsk, 630117, Russia
Show Author Information

Abstract

Background

Himalayan Griffons (Gyps himalayensis), large scavenging raptors widely distributed in Qinghai-Tibetan Plateau, have evolved a remarkable ability to feed on carcasses without suffering any adverse effects. The gut microbiome plays an important role in animal physiological and pathological processes, and has also been found to play a health protective role in the vulture adaptation to scavenging. However, the microbial taxonomic diversity (including nonculturable and culturable microbes), functions, and metabolites related to Himalayan Griffons have not been fully explored.

Methods

In the present study, the 28 fecal samples of the Himalayan Griffons and 8 carrion samples were collected and sequenced using high-throughput 16S rRNA gene sequencing methods to analyze the composition and functional structures of the microbiomes. Twelve fecal samples of the Himalayan Griffons were analyzed using untargeted Liquid Chromatography Mass Spectroscopy (LC–MS) to identify metabolites. We used different culture conditions to grow Himalayan Griffons gut microbes. Inhibitory effects of gut beneficial bacteria on 5 common pathogenic bacteria were also tested using the Oxford cup method.

Results

According to the results of the culture-independent method, a high abundance of four major phyla in Himalayan Griffons were identified, including Fusobacteria, Firmicutes, Bacteroidetes, and Proteobacteria. The most abundant genera were Fusobacterium, followed by Clostridium_sensu_stricto_1, Cetobacterium, Epulopiscium, and Bacteroides. The predicted primary functional categories of the Himalayan Griffons' gut microbiome were associated with carbohydrate and amino acid metabolism, replication and repair, and membrane transport. LC–MS metabolomic analysis showed a total of 154 metabolites in all the fecal samples. Cultivation yielded 184 bacterial isolates with Escherichia coli, Enterococcus faecium, Enterococcus hirae, and Paeniclostridium sordellii as most common isolates. Moreover, 7 potential beneficial gut bacteria isolated showed certain inhibition to 5 common pathogenic bacteria.

Conclusions

Our findings broaden and deepen the understanding of Himalayan Griffons' gut microbiome, and highlighted the importance of gut microbiome-mediated adaptation to scavenging habits. In particular, our results highlighted the protective role of gut beneficial bacteria in the Himalayan Griffons against pathogenic bacteria that appear in rotten food resources.

Keywords

MicrobiomeCultureAvian scavengersPathogensVultures

References

 

Arroyo FA, Pawlowska TE, Choat JH, Clements KD, Angert ER. Recombination contributes to population diversification in the polyploid intestinal symbiont Epulopiscium sp. type B. ISME J. 2019;13: 1084-97.
Crossref Google Scholar
 

Barnes A, Kaur A, Augenbraun M. An unusual presentation of prostatic abscess due to Actinomyces turicensis and Peptostreptococcus. Cureus. 2020;12: e8665.
Google Scholar
 

Berry D. The emerging view of Firmicutes as key fibre degraders in the human gut. Environ Microbiol. 2016;18: 2081-3.
Crossref Google Scholar
 
BirdLife International. Gyps himalayensis (amended version of 2017 assessment). The IUCN red list of threatened species 2017: e. T22695215A118594518. 2017. htthttps://doi.org/10.2305/IUCN.UK.2017-3.RLTS.T22695215A118594518.en. Accessed 10 Sept 2020.
Crossref
 

Blumstein DT, Rangchi TN, Briggs T, de Andrade FS, Natterson-Horowitz B. A systematic review of carrion eaters' adaptations to avoid sickness. J Wildl Dis. 2017;53: 577-81.
Crossref Google Scholar
 

Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QⅡME allows analysis of high-throughput community sequencing data. Nat Method. 2010;7: 335-6.
Crossref Google Scholar
 

Chung O, Jin S, Cho YS, Lim J, Kim H, Jho S, et al. The first whole genome and transcriptome of the cinereous vulture reveals adaptation in the gastric and immune defense systems and possible convergent evolution between the Old and New World vultures. Genome Biol. 2015;16: 215.
Crossref Google Scholar
 

Colston TJ, Jackson CR. Microbiome evolution along divergent branches of the vertebrate tree of life: what is known and unknown. Mol Ecol. 2016;25: 3776-800.
Crossref Google Scholar
 

David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505: 559-63.
Crossref Google Scholar
 

de Paepe K, Kerckhof FM, Verspreet J, Courtin CM, Van de Wiele T. Inter-individual differences determine the outcome of wheat bran colonization by the human gut microbiome. Environ Microbiol. 2017;19: 3251-67.
Crossref Google Scholar
 

Diakou A, Norte AC, de Carvalho IL, Núncio S, Nováková M, Kautman M, et al. Ticks and tick-borne pathogens in wild birds in Greece. Parasitol Res. 2016;115: 2011-6.
Crossref Google Scholar
 

Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Method. 2013;10: 996-8.
Crossref Google Scholar
 

Gao H, Jiang Q, Ji H, Ning J, Li C, Zheng H. Type 1 diabetes induces cognitive dysfunction in rats associated with alterations of the gut microbiome and metabolomes in serum and hippocampus. BBA-Mol Basis Dis. 2019;1865: 165541.
Crossref Google Scholar
 

Garg S, Kaul SC, Wadhwa R. Cucurbitacin B and cancer intervention: chemistry, biology and mechanisms. Int J Oncol. 2018;52: 19-37.
Crossref Google Scholar
 

Ghonimy A, Zhang DM, Farouk MH, Wang Q. The impact of carnitine on dietary fiber and gut bacteria metabolism and their mutual interaction in monogastrics. Int J Mol Sci. 2018;19: 1008.
Crossref Google Scholar
 

Grigor'eva IN. Gallstone disease, obesity and the Firmicutes/Bacteroidetes ratio as a possible biomarker of gut dysbiosis. J Pers Med. 2021;11: 13.
Crossref Google Scholar
 

Hird SM. Evolutionary biology needs wild microbiomes. Front Microbiol. 2017;8: 725.
Crossref Google Scholar
 

Houston DC, Cooper JE. The digestive tract of the whiteback griffon vulture and its role in disease transmission among wild ungulates. J Wildl Dis. 1975;11: 306-13.
Crossref Google Scholar
 

Huang P, Zhang Y, Xiao K, Jiang F, Wang H, Tang D, et al. The chicken gut metagenome and the modulatory effects of plant-derived benzylisoquinoline alkaloids. Microbiome. 2018;6: 211.
Crossref Google Scholar
 

Huang G, Wang X, Hu Y, Wu Q, Nie Y, Dong J, et al. Diet drives convergent evolution of gut microbiomes in bamboo-eating species. Sci China Life Sci. 2021;64: 88-95.
Crossref Google Scholar
 

Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science. 2014;346: 1320-31.
Crossref Google Scholar
 

Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. Human nutrition, the gut microbiome and the immune system. Nature. 2011;474: 327-36.
Crossref Google Scholar
 

Keenan SW, Engel AS, Elsey RM. The alligator gut microbiome and implications for archosaur symbioses. Sci Rep. 2013;3: 2877.
Crossref Google Scholar
 

Kelly D, Yang L, Pei Z. Gut microbiota, Fusobacteria, and colorectal cancer. Diseases. 2018;6: 109.
Crossref Google Scholar
 

Kocijan I, Prukner-Radovčić E, Beck R, Galov A, Marinculić A, Sušić G. Microflora and internal parasites of the digestive tract of Eurasian griffon vultures (Gyps fulvus) in Croatia. Eur J Wildl Res. 2009;55: 71-4.
Crossref Google Scholar
 

Kogut MH. Issues and consequences of using nutrition to modulate the avian immune response. J Appl Poultry Res. 2017;26: 605-12.
Crossref Google Scholar
 

Kohl KD. Diversity and function of the avian gut microbiota. J Comp Physiol B. 2012;182: 591-602.
Crossref Google Scholar
 

Kohl KD, Connelly JW, Dearing MD, Forbey JS. Microbial detoxification in the gut of a specialist avian herbivore, the Greater Sage-Grouse. FEMS Microbiol Lett. 2016;363: fnw144.
Crossref Google Scholar
 

Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35: 1547-9.
Crossref Google Scholar
 

Lagier JC, Armougom F, Million M, Hugon P, Pagnier I, Robert C, et al. Microbial culturomics: paradigm shift in the human gut microbiome study. Clin Microbiol Infect. 2012;18: 1185-93.
Crossref Google Scholar
 

Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31: 814-21.
Crossref Google Scholar
 

Lee WY. Avian gut microbiota and behavioral studies. Korean J Ornithol. 2015;22: 1-11.
Google Scholar
 

Lee WJ, Hase K. Gut microbiota-generated metabolites in animal health and disease. Nat Chem Biol. 2014;10: 416-24.
Crossref Google Scholar
 

Levin D, Raab N, Pinto Y, Rothschild D, Zanir G, Godneva A, et al. Diversity and functional landscapes in the microbiota of animals in the wild. Science. 2021;372: e5352.
Crossref Google Scholar
 

Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, et al. Evolution of mammals and their gut microbes. Science. 2008;320: 1647-51.
Crossref Google Scholar
 

Lu X, Ke D, Zeng X, Gong G, Ci R. Status, ecology, and conservation of the Himalayan griffon Gyps himalayensis (Aves, Accipitridae) in the Tibetan plateau. Ambio. 2009;38: 166-73.
Crossref Google Scholar
 

Margalida A, Oliva-Vidal P. The shadow of diclofenac hangs over European vultures. Nat Ecol Evol. 2017;1: 1050.
Crossref Google Scholar
 
Mateos-Hernández L, Crespo E, de la Fuente J, de la Lastra JMP. Identification of key molecules involved in the protection of vultures against pathogens and toxins. In: Radis-Baptista G, editor. An integrated view of the molecular recognition and toxinology: from analytical procedures to biomedical applications. Rijeka: InTech; 2013. p. 241-65.https://doi.org/10.5772/54191
Crossref
 

Meadows JA, Wargo MJ. Carnitine in bacterial physiology and metabolism. Microbiology. 2015;161: 1161-74.
Crossref Google Scholar
 

Meng X, Lu S, Lai XH, Wang Y, Wen Y, Jin D, et al. Actinomyces liubingyangii sp. nov. isolated from the vulture Gypaetus barbatus. Int J Syst Evol Microbiol. 2017a;67: 1873-9.
Crossref Google Scholar
 

Meng X, Lu S, Wang Y, Lai XH, Wen Y, Jin D, et al. Actinomyces vulturis sp. nov., isolated from Gyps himalayensis. Int J Syst Evol Microbiol. 2017b;67: 1720-6.
Crossref Google Scholar
 

Meng X, Lu S, Yang J, Jin D, Wang X, Bai X, et al. Metataxonomics reveal vultures as a reservoir for Clostridium perfringens. Emerg Microbes Infect. 2017c;6: e9.
Crossref Google Scholar
 

Meng X, Lai XH, Lu S, Liu S, Chen C, Zhou D, et al. Actinomyces tangfeifanii sp. nov., isolated from the vulture Aegypius monachus. Int J Syst Evol Microbiol. 2018;68: 3701-6.
Crossref Google Scholar
 

Miyake S, Ngugi DK, Stingl U. Phylogenetic diversity, distribution, and cophylogeny of giant bacteria (Epulopiscium) with their surgeonfish hosts in the Red Sea. Front Microbiol. 2016;7: 285.
Crossref Google Scholar
 

Moleón M, Sánchez-Zapata JA, Margalida A, Carrete M, Owen-Smith N, Donázar JA. Humans and scavengers: the evolution of interactions and ecosystem services. Bioscience. 2014;64: 394-403.
Crossref Google Scholar
 

Ogada D, Shaw P, Beyers RL, Buij R, Murn C, Thiollay JM, et al. Another continental vulture crisis: Africa's vultures collapsing toward extinction. Conserv Lett. 2016;9: 89-97.
Crossref Google Scholar
 

Padayachee T, Nzuza N, Chen W, Nelson DR, Syed K. Impact of lifestyle on cytochrome P450 monooxygenase repertoire is clearly evident in the bacterial phylum Firmicutes. Sci Rep. 2020;10: 13982.
Crossref Google Scholar
 

Pinevich AV, Andronov EE, Pershina EV, Pinevich AA, Dmitrieva HY. Testing culture purity in prokaryotes: criteria and challenges. Antonie Van Leeuwenhoek. 2018;111: 1509-21.
Crossref Google Scholar
 

Plaza PI, Blanco G, Madariaga MJ, Boeri E, Teijeiro ML, Bianco G, et al. Scavenger birds exploiting rubbish dumps: pathogens at the gates. Transbound Emerg Dis. 2019;66: 873-81.
Crossref Google Scholar
 

Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41: D590-6.
Crossref Google Scholar
 

Ramirez C, Coronado J, Silva A, Romero J. Cetobacterium is a major component of the microbiome of giant Amazonian fish (Arapaima gigas) in Ecuador. Animals. 2018;8: 189.
Crossref Google Scholar
 

Roggenbuck M, Bærholm Schnell I, Blom N, Bælum J, Bertelsen MF, Sicheritz-Pontén T, et al. The microbiome of New World vultures. Nat Commun. 2014;5: 5498.
Crossref Google Scholar
 

Rubinstein MR, Wang X, Liu W, Hao Y, Cai G, Han YW. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe. 2013;14: 195-206.
Crossref Google Scholar
 

Simon K, Verwoolde MB, Zhang J, Smidt H, de Vries RG, Kemp B, et al. Long-term effects of early life microbiota disturbance on adaptive immunity in laying hens. Poult Sci. 2016;95: 1543-54.
Crossref Google Scholar
 

Smiddy M, Sleator RD, Patterson MF, Hill C, Kelly AL. Role for compatible solutes glycine betaine and L-carnitine in listerial barotolerance. Appl Environ Microbiol. 2004;70: 7555-7.
Crossref Google Scholar
 

Trevelline BK, Fontaine SS, Hartup BK, Kohl KD. Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices. P Roy Soc B-Biol Sci. 2019;286: 20182448.
Crossref Google Scholar
 

Waite DW, Taylor MW. Characterizing the avian gut microbiota: membership, driving influences, and potential function. Front Microbiol. 2014;5: 223.
Crossref Google Scholar
 

Waite DW, Taylor MW. Exploring the avian gut microbiota: current trends and future directions. Front Microbiol. 2015;6: 673.
Crossref Google Scholar
 

Wei F, Wu Q, Hu Y, Huang G, Nie Y, Yan L. Conservation metagenomics: a new branch of conservation biology. Sci China Life Sci. 2019;62: 168-78.
Crossref Google Scholar
 

Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334: 105-8.
Crossref Google Scholar
 

Yao R, Xu L, Lu G, Zhu L. Evaluation of the function of wild animal gut microbiomes using next-generation sequencing and bioinformatics and its relevance to animal conservation. Evol Bioinform Online. 2019;15: 1176934319848438.
Crossref Google Scholar
 

Zepeda Mendoza ML, Roggenbuck M, Manzano-Vargas K, Hansen LH, Brunak S, Gilbert MTP, et al. Protective role of the vulture facial skin and gut microbiomes aid adaptation to scavenging. Acta Vet Scand. 2018;60: 61.
Crossref Google Scholar
 

Zhai Q, Yin R, Yu L, Wang G, Tian F, Yu R, et al. Screening of lactic acid bacteria with potential protective effects against cadmium toxicity. Food Control. 2015;54: 23-30.
Crossref Google Scholar
 

Zhang G, Li C, Li Q, Li B, Larkin DM, Lee C, et al. Comparative genomics reveals insights into avian genome evolution and adaptation. Science. 2014;346: 1311-20.
Crossref Google Scholar
 

Zhou C, Wang G, Yu H, Geng Y, Wu W, Tu H, et al. Genome-wide analysis reveals the genomic features of the turkey vulture (Cathartes aura) as a scavenger. Mol Genet Genom. 2019;294: 679-92.
Crossref Google Scholar
Avian Research
Volume 12 Issue 1,
January 2021
Article number: 52
DOI: 10.1186/s40657-021-00287-0
Cite this article:
Wang W, Gao X, Zheng S, et al. The gut microbiome and metabolome of Himalayan Griffons (Gyps himalayensis): insights into the adaptation to carrion-feeding habits in avian scavengers. Avian Research, 2021, 12(1): 52. https://doi.org/10.1186/s40657-021-00287-0

884

Views

29

Downloads

9

Crossref

8

Web of Science

8

Scopus

0

CSCD

Altmetrics
Received: 29 April 2021
Accepted: 30 September 2021
Published: 18 October 2021
© The Author(s) 2021.

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-sa/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
Return