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Volume 48 Issue 9
Sep.  2021
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Article Contents

Comparative study of gut microbiota from captive and confiscated-rescued wild pangolins

doi: 10.1016/j.jgg.2021.07.009
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We thank English-native speakers Dr. John Blackwell and his colleagues for honing the English of the manuscript. The research was supported by the National Science Fund for Distinguished Young Scholars, China (31925006), the Major Science and Technology Project in Yunnan Province of China, China (202001BB050001), the Second Tibetan Plateau Scientific Expedition and Research (STEP) program, China (2019QZKK0503), and the Animal Branch of the Germplasm Bank of Wild Species, Chinese Academy of Sciences.

  • Received Date: 2021-05-17
  • Revised Date: 2021-07-11
  • Accepted Date: 2021-07-21
  • Publish Date: 2021-08-05
  • Pangolins are among the most critically endangered animals due to widespread poaching and worldwide trafficking. Captive breeding is considered to be one way to protect them and increase the sizes of their populations. However, comparative studies of captive and wild pangolins in the context of gut microbiota are rare. Here, the gut microbiome of captive and confiscated-rescued wild pangolins is compared, and the effects of different periods of captivity and captivity with and without antibiotic treatment are considered. We show that different diets and periods of captivity, as well as the application of antibiotic therapy, can alter gut community composition and abundance in pangolins. Compared to wild pangolins, captive pangolins have an increased capacity for chitin and cellulose/hemicellulose degradation, fatty acid metabolism, and short-chain fatty acid synthesis, but a reduced ability to metabolize exogenous substances. In addition to increasing the ability of the gut microbiota to metabolize nutrients in captivity, captive breeding imposes some risks for survival by resulting in a greater abundance of antibiotic resistance genes and virulence factors in captive pangolins than in wild pangolins. Our study is important for the development of guidelines for pangolin conservation, including health assessment, disease prevention, and rehabilitation of wild pangolin populations.
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  • Ahmed, A.M., Motoi, Y., Sato, M., Maruyama, A., Watanabe, H., Fukumoto, Y., Shimamoto, T., 2007. Zoo animals as reservoirs of gram-negative bacteria harboring integrons and antimicrobial resistance genes. Appl. Environ. Microbiol. 73, 6686-6690.
    Alcock, B.P., Raphenya, A.R., Lau, T.T.Y., Tsang, K.K., Bouchard, M., Edalatmand, A., Huynh, W., Nguyen, A.V., Cheng, A.A., Liu, S., 2020. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res. 48, 517-525.
    Anderson, M.J., 2005. PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Ecol. Monogr. 83, 557-574.
    Araki, H., Cooper, B., Blouin, M.S., 2007. Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318, 100-103.
    Baquero, F., Martinez, J.L., Canton, R., 2008. Antibiotics and antibiotic resistance in water environments. Curr. Opin. Biotechnol. 19, 260-265.
    Barelli, C., Albanese, D., Donati, C., Pindo, M., Dallago, C., Rovero, F., Cavalieri, D., Tuohy, K.M., Hauffe, H.C., De Filippo, C., 2015. Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: implications for conservation. Sci. Rep. 5, 14862.
    Bolger, A.M., Lohse, M., Usadel, B., 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120.
    Borbon-Garcia, A., Reyes, A., Vives-Florez, M., Caballero, S., 2017. Captivity shapes the gut microbiota of andean bears: insights into health surveillance. Front. Microbiol. 8, 1316.
    Bravo, J.A., Julio-Pieper, M., Forsythe, P., Kunze, W., Dinan, T.G., Bienenstock, J., Cryan, J.F., 2012. Communication between gastrointestinal bacteria and the nervous system. Curr. Opin. Pharmacol. 12, 667-672.
    Brucker, R.M., Bordenstein, S.R., 2012. Speciation by symbiosis. Trends Ecol. Evol. 27, 443-451.
    Bruggemann, H., Baumer, S., Fricke, W.F., Wiezer, A., Liesegang, H., Decker, I., Herzberg, C., Martinez-Arias, R., Merkl, R., Henne, A., 2003. The genome sequence of Clostridium tetani, the causative agent of tetanus disease. Proc. Natl. Acad. Sci. U. S. A. 100, 1316-1321.
    Buchfink, B., Xie, C., Huson, D.H., 2015. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59-60.
    Cabana, F., Plowman, A., Van Nguyen, T., Chin, S.C., Wu, S.L., Lo, H.Y., Watabe, H., Yamamoto, F., 2017. Feeding Asian pangolins: an assessment of current diets fed in institutions worldwide. Zoo Biol. 36, 298-305.
    Cabana, F., Tay, C., 2020. The addition of soil and chitin into Sunda pangolin (Manis javanica) diets affect digestibility, faecal scoring, mean retention time and body weight. Zoo Biol. 39, 29-36.
    Candela, M., Maccaferri, S., Turroni, S., Carnevali, P., Brigidi, P., 2010. Functional intestinal microbiome, new frontiers in prebiotic design. Int. J. Food Microbiol. 140, 93-101.
    Challender, D., Willcox, D.H.A., Panjang, E., Lim, N., Nash, H., Heinrich, S., Chong, J., 2019a. Manis javanica. The IUCN Red List of Threatened Species 2019. e.T12763A123584856.
    Challender, D., Wu, S., Kaspal, P., Khatiwada, A., Ghose, A., Ching-Min Sun, N., Mohapatra, R.K., Laxmi Suwal, T., 2019b. Manis pentadactyla (errata version published in 2020). The IUCN Red List of Threatened Species 2019. e.T12764A168392151.
    Challender, D.W.S., 2011. Asian pangolins: increasing affluence driving hunting pressure. Traffic Bull. 23, 92-93.
    Challender, D.W.S., Harrop, S.R., MacMillan, D.C., 2015. Understanding markets to conserve trade-threatened species in CITES. Biol. Conserv. 187, 249-259.
    Chen, L., Zheng, D., Liu, B., Yang, J., Jin, Q., 2016. VFDB 2016: hierarchical and refined dataset for big data analysis-10 years on. Nucleic Acids Res. 44, 694-697.
    Cheng, W.D., Xing, S., Bonebrake, T.C., 2017. Recent pangolin seizures in China reveal priority areas for intervention. Conserv. Lett. 10, 757-764.
    Chin, S.C., Lien, C.Y., Chan, Y.T., Chen, C.L., Yang, Y.C., Yeh, L.S., 2012. Monitoring the gestation period of rescued Formosan pangolin (Manis pentadactyla) with progesterone radioimmunoassay. Zoo Biol. 31, 479-489.
    Choo, S.W., Rayko, M., Tan, T.K., Hari, R., Komissarov, A., Wee, W.Y., Yurchenko, A.A., Kliver, S., Tamazian, G., Antunes, A., 2016. Pangolin genomes and the evolution of mammalian scales and immunity. Genome Res. 26, 1312-1322.
    Cotillard, A., Kennedy, S.P., Kong, L.C., Prifti, E., Pons, N., Le Chatelier, E., Almeida, M., Quinquis, B., Levenez, F., Galleron, N., 2013. Dietary intervention impact on gut microbial gene richness. Nature 500, 585-588.
    Davies, Y.M., Cunha, M.P., Oliveira, M.G., Oliveira, M.C., Philadelpho, N., Romero, D.C., Milanelo, L., Guimaraes, M.B., Ferreira, A.J., Moreno, A.M., 2016. Virulence and antimicrobial resistance of Klebsiella pneumoniae isolated from passerine and psittacine birds. Avian Pathol. 45, 194-201.
    Delsuc, F., Metcalf, J.L., Wegener Parfrey, L., Song, S.J., Gonzalez, A., Knight, R., 2014. Convergence of gut microbiomes in myrmecophagous mammals. Mol. Ecol. 23, 1301-1317.
    Eckburg, P.B., Bik, E.M., Bernstein, C.N., Purdom, E., Dethlefsen, L., Sargent, M., Gill, S.R., Nelson, K.E., Relman, D.A., 2005. Diversity of the human intestinal microbial flora. Science 308, 1635-1638.
    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.
    Frankel, J.S., Mallott, E.K., Hopper, L.M., Ross, S.R., Amato, K.R., 2019. The effect of captivity on the primate gut microbiome varies with host dietary niche. Am. J. Primatol. 81, e23061.
    Fraser, D.J., 2008. How well can captive breeding programs conserve biodiversity? A review of salmonids. Evol. Appl. 1, 535-586.
    Gantner, S., Andersson, A.F., Alonso-Saez, L., Bertilsson, S., 2011. Novel primers for 16S rRNA-based archaeal community analyses in environmental samples. J. Microbiol. Methods 84, 12-18.
    Gibson, K.M., Nguyen, B.N., Neumann, L.M., Miller, M., Buss, P., Daniels, S., Ahn, M.J., Crandall, K.A., Pukazhenthi, B., 2019. Gut microbiome differences between wild and captive black rhinoceros — implications for rhino health. Sci. Rep. 9, 7570.
    Gothwal, R., Shashidhar, T., 2015. Antibiotic pollution in the environment: A review. Clean-Soil Air Water 43, 479-489.
    Guo, W., Mishra, S., Wang, C., Zhang, H., Ning, R., Kong, F., Zeng, B., Zhao, J., Li, Y., 2019. Comparative study of gut microbiota in wild and captive giant pandas (Ailuropoda melanoleuca). Genes 10, 827.
    Hall, M., Beiko, R.G., 2018. 16S rRNA gene analysis with QIIME2. Methods Mol. Biol. 1849, 113-129.
    Heinrich, S., Wittmann, T.A., Prowse, T.A.A., Ross, J.V., Delean, S., Shepherd, C.R., Cassey, P., 2016. Where did all the pangolins go? International CITES trade in pangolin species. Glob. Ecol. Conserv. 8, 241-253.
    Holt, W.V., Pickard, A.R., Prather, R.S., 2004. Wildlife conservation and reproductive cloning. Reproduction 127, 317-324.
    Hsieh, H.M., Lee, J.C., Wu, J.H., Chen, C.A., Chen, Y.J., Wang, G.B., Chin, S.C., Wang, L.C., Linacre, A., Tsai, L.C., 2011. Establishing the pangolin mitochondrial D-loop sequences from the confiscated scales. Forensic Sci. Int. Genet. 5, 303-307.
    , Hao, Z.Q., F. L, 2020. Genomic consequences of population decline in critically endangered pangolins and their demographic histories. Natl. Sci. Rev. 7, 798-814.
    Hua, L., Gong, S., Wang, F., Li, W., Ge, Y., Li, X., Hou, F., 2015. Captive breeding of pangolins: current status, problems and future prospects. Zookeys 507, 99-114.
    Huson, D.H., Beier, S., Flade, I., Gorska, A., El-Hadidi, M., Mitra, S., Ruscheweyh, H.J., Tappu, R., 2016. MEGAN community edition-interactive exploration and analysis of large-scale microbiome sequencing data. PLoS Comput. Biol. 12, e1004957.
    Jin, M., Li, D., Ji, R., Liu, W., Xu, X., Li, Y., 2020. Changes in intestinal microflora in digestive tract diseases during pregnancy. Arch. Gynecol. Obstet. 301, 243-249.
    Jumpertz, R., Le, D.S., Turnbaugh, P.J., Trinidad, C., Bogardus, C., Gordon, J.I., Krakoff, J., 2011. Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Am. J. Clin. Nutr. 94, 58-65.
    Li, H., Durbin, R., 2010. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589-595.
    Li, W., Godzik, A., 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658-1659.
    Li, D., Liu, C.M., Luo, R., Sadakane, K., Lam, T.W., 2015. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31, 1674-1676.
    Liu, Y., Weng, Q., 2014. Fauna in decline: plight of the pangolin. Science 345, 884.
    Luczon, A.U., Ong, P.S., Quilang, J.P., Fontanilla, I.K.C., 2016. Determining species identity from confiscated pangolin remains using DNA barcoding. Mitochondrial DNA B. 1, 763-766.
    Ma, L., Li, B., Jiang, X.T., Wang, Y.L., Xia, Y., Li, A.D., Zhang, T., 2017. Catalogue of antibiotic resistome and host-tracking in drinking water deciphered by a large scale survey. Microbiome 5, 154.
    Marx, A., Backes, C., Meese, E., Lenhof, H.P., Keller, A., 2016. EDISON-WMW: exact dynamic programing solution of the Wilcoxon-Mann-Whitney test. Genom. Proteom. Bioinf. 14, 55-61.
    McDougall, F., Boardman, W., Gillings, M., Power, M., 2019. Bats as reservoirs of antibiotic resistance determinants: A survey of class 1 integrons in Grey-headed Flying Foxes (Pteropus poliocephalus). Infect. Genet. Evol. 70, 107-113.
    McKenzie, V.J., Song, S.J., Delsuc, F., Prest, T.L., Oliverio, A.M., Korpita, T.M., Alexiev, A., Amato, K.R., Metcalf, J.L., Kowalewski, M., 2017. The effects of captivity on the mammalian gut microbiome. Integr. Comp. Biol. 57, 690-704.
    McMurdie, P.J., Holmes, S., 2013. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8, e61217.
    Mikich, S.B., Liebsch, D., 2014. Damage to forest plantations by tufted capuchins (Sapajus nigritus): Too many monkeys or not enough fruits. For. Ecol. Manage. 314, 9-16.
    Mohapatra, R.K., Panda, S., 2014. Husbandry, behaviour and conservation breeding of Indian pangolin. Folia Zool. 63, 73-80.
    Myers, G.S., Rasko, D.A., Cheung, J.K., Ravel, J., Seshadri, R., DeBoy, R.T., Ren, Q., Varga, J., Awad, M.M., Brinkac, L.M., 2006. Skewed genomic variability in strains of the toxigenic bacterial pathogen, Clostridium perfringens. Genome Res. 16, 1031-1040.
    Nash, H.C., Wirdateti, Low, G.W., Choo, S.W., Chong, J.L., Semiadi, G., Hari, R., Sulaiman, M.H., Turvey, S.T., Evans, T.A., 2018. Conservation genomics reveals possible illegal trade routes and admixture across pangolin lineages in Southeast Asia. Conserv. Genet. 19, 1083-1095.
    Nijman, V., Zhang, M.X., Shepherd, C.R., 2016. Pangolin trade in the Mong La wildlife market and the role of Myanmar in the smuggling of pangolins into China. Glob. Ecol. Conserv. 5, 118-126.
    Ning, Y., Qi, J., Dobbins, M.T., Liang, X., Wang, J., Chen, S., Ma, J., Jiang, G., 2020. Comparative analysis of microbial community structure and function in the gut of wild and captive Amur tiger. Front. Microbiol. 11, 1665.
    Park, S.Y., Lee, K., Cho, Y., Lim, S.R., Kwon, H., Han, J.E., Kim, J.H., 2020. Emergence of third-generation cephalosporin-resistant Morganella morganii in a captive breeding dolphin in South Korea. Animals (Basel) 10, 2052.
    Pechine, S., Hennequin, C., Boursier, C., Hoys, S., Collignon, A., 2013. Immunization using GroEL decreases Clostridium difficile intestinal colonization. PLoS One 8, 81112.
    Pel, R., 1989. Chitin degradation by Clostridium sp. strain 9.1 in mixed cultures with saccharolytic and sulfate-reducing bacteria. FEMS Microbiol. Lett. 62, 191-200.
    Richardson, P.M., de Been, M., Lanza, V.F., de Toro, M., Scharringa, J., Dohmen, W., Du, Y., Hu, J., Lei, Y., Li, N., 2014. Dissemination of cephalosporin resistance genes between Escherichia coli strains from farm animals and humans by specific plasmid lineages. PLoS Genet. 10, 1004776.
    Rognes, T., Flouri, T., Nichols, B., Quince, C., Mahe, F., 2016. VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, e2584.
    Round, J.L., Mazmanian, S.K., 2009. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9, 313-323.
    Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541.
    Sebaihia, M., Wren, B.W., Mullany, P., Fairweather, N.F., Minton, N., Stabler, R., Thomson, N.R., Roberts, A.P., Cerdeno-Tarraga, A.M., Wang, H., 2006. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat. Genet. 38, 779-786.
    Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W.S., Huttenhower, C., 2011. Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60.
    Shimizu, T., Ohtani, K., Hirakawa, H., Ohshima, K., Yamashita, A., Shiba, T., Ogasawara, N., Hattori, M.K., Hayashi, S.H., 2002. Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater. Proc. Natl. Acad. Sci. U. S. A. 99, 996-1001.
    Singer, A.C., Shaw, H., Rhodes, V., Hart, A., 2016. Review of antimicrobial resistance in the environment and its relevance to environmental regulators. Front. Microbiol. 7, 1728.
    Sun, N.C., Lo, F.H., Chen, B.Y., Yu, H.Y., Liang, C.C., Lin, C.C., Chin, S.C., Li, H.F., 2020. Digesta retention time and recovery rates of ants and termites in Chinese pangolins (Manis pentadactyla). Zoo Biol. 39, 168-175.
    Thomas, C.M., Nielsen, K.M., 2005. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat. Rev. Microbiol. 3, 711-721.
    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.
    Warton, D.I., Wright, S.T., Wang, Y., 2012. Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol. Evol. 3, 89-101.
    Whitman, W.B., Rainey, F., Kämpfer, P., Trujillo, M., Chun, J., DeVos, P., Hedlund, B., Dedysh, S., 2016. Cellulosilyticum. BMSAB 1-4.
    Yan, D., Hu, D., Li, K., Li, B., Zeng, X., Chen, J., Li, Y., Wronski, T., 2021. Effects of chronic stress on the fecal microbiome of malayan pangolins (Manis javanica) rescued from the illegal wildlife trade. Curr. Microbiol. 78, 1017-1025.
    Yang, L., Chen, M., Challender, D.W.S., Waterman, C., Zhang, C., Huo, Z., Liu, H., Luan, X., 2018. Historical data for conservation: reconstructing range changes of Chinese pangolin (Manis pentadactyla) in eastern China (1970–2016). Proc. Biol. Sci. 285, 20181084.
    Zhang, C., Li, S., Yang, L., Huang, P., Li, W., Wang, S., Zhao, G., Zhang, M., Pang, X., Yan, Z., 2013. Structural modulation of gut microbiota in life-long calorie-restricted mice. Nat. Commun. 4, 2163.
    Zhang, H., Miller, M.P., Yang, F., Chan, H.K., Gaubert, P., Ades, G., Fischer, G.A., 2015. Molecular tracing of confiscated pangolin scales for conservation and illegal trade monitoring in Southeast Asia. Glob. Ecol. Conserv. 4, 414-422.
    Zhang, H., Yohe, T., Huang, L., Entwistle, S., Wu, P., Yang, Z., Busk, P.K., Xu, Y., Yin, Y., 2018. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 46, W95-W101.
    Zhao, L., Wang, G., Siegel, P., He, C., Wang, H.Z., Zhao, W.J., Zhai, Z.X., Tian, F.W., Zhao, J.X., Zhang, H., 2013. Quantitative genetic background of the host influences gut microbiomes in chickens. Sci. Rep. 3, 1163.
    Zhu, W., Lomsadze, A., Borodovsky, M., 2010. Ab initio gene identification in metagenomic sequences. Nucleic Acids Res. 38, 132.
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