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Ambient temperature alters body size and gut microbiota of Xenopus tropicalis

  • Jiaying Li
  • Junpeng Rui
  • Yulong Li
  • Na Tang
  • Songping Zhan
  • Jianping JiangEmail author
  • Xiangzhen LiEmail author
Research Paper
  • 16 Downloads

Abstract

Temperature is important to determine physiological status of ectotherms. However, it is still not fully understood how amphibians and their symbiotic microbiota acclimate to ambient temperature. In this study, we investigated the changes of gut microbiota of Xenopus tropicalis at different temperatures under controlled laboratory conditions. The results showed that microbial communities were distinct and shared only a small overlap among froglet guts, culture water and food samples. Furthermore, the dominant taxa harbored in the gut exhibited low relative abundance in water and food. It indicates that bacterial taxa selected by amphibian gut were generally of low abundance in the external environment. Temperature could affect beta-diversity of gut microbiota in terms of phylogenetic distance, but it did not affect alpha diversity. The composition of gut microbiota was similar in warm and cool treatments. However, signature taxa in different temperature environments were identified. The relationships between temperature, gut microbiota and morphology traits of X. tropicalis revealed in this study help us to predict the consequences of environmental changes on ectothermic animals.

gut microbiota Xenopus tropicalis temperature body size thermal adaptation 

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Acknowledgements

This work was supported by the National Key Program of Research and Development, Ministry of Science and Technology of China (2016YFC0503200), Sichuan Province Science and Technology Project (2017SZ0004), the 13th Five-year Informatization Plan of Chinese Academy of Sciences (XXH13503-03-106), Open Fund of Key Laboratory of Environmental and Applied Microbiology CAS (KLCAS-2017-3, KLCAS-2016-03), and China Biodiversity Observation Networks (Sino BON).

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Ambient temperature alters body size and gut microbiota of Xenopus tropicalis
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References

  1. Atkinson, D. (1994). Temperature and organism size—a biological law for ectotherms? Adv Ecol Res 25, 1–58.CrossRefGoogle Scholar
  2. Bajaj, J.S., Hylemon, P.B., Ridlon, J.M., Heuman, D.M., Daita, K., White, M.B., Monteith, P., Noble, N.A., Sikaroodi, M., and Gillevet, P.M. (2012a). Colonic mucosal microbiome differs from stool microbiome in cirrhosis and hepatic encephalopathy and is linked to cognition and inflammation. Am J Physiol Gastrointest Liver Physiol 303, G675–G685.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bajaj, J.S., Ridlon, J.M., Hylemon, P.B., Thacker, L.R., Heuman, D.M., Smith, S., Sikaroodi, M., and Gillevet, P.M. (2012b). Linkage of gut microbiome with cognition in hepatic encephalopathy. Am J Physiol Gastrointest Liver Physiol 302, G168–G175.PubMedCrossRefGoogle Scholar
  4. Bajaj, J.S., Heuman, D.M., Hylemon, P.B., Sanyal, A.J., White, M.B., Monteith, P., Noble, N.A., Unser, A.B., Daita, K., Fisher, A.R., et al. (2014). Altered profile of human gut microbiome is associated with cirrhosis and its complications. J Hepatol 60, 940–947.PubMedCrossRefGoogle Scholar
  5. Banas, J.A., Loesche, W.J., and Nace, G.W. (1988). Classification and distribution of large intestinal bacteria in nonhibernating and hibernating leopard frogs (Rana pipiens). Appl Environ Microbiol 54, 2305–2310.PubMedPubMedCentralGoogle Scholar
  6. Bergheim, I., Weber, S., Vos, M., Krämer, S., Volynets, V., Kaserouni, S., McClain, C.J., and Bischoff, S.C. (2008). Antibiotics protect against fructose-induced hepatic lipid accumulation in mice: role of endotoxin. J Hepatol 48, 983–992.PubMedCrossRefGoogle Scholar
  7. Bestion, E., Jacob, S., Zinger, L., Di Gesu, L., Richard, M., White, J., and Cote, J. (2017). Climate warming reduces gut microbiota diversity in a vertebrate ectotherm. Nat Ecol Evol 1, 0161.CrossRefGoogle Scholar
  8. Bizer, J.R. (1978). Growth rates and size at metamorphosis of high elevation populations of Ambystoma tigrinum. Oecologia 34, 175–184.PubMedCrossRefGoogle Scholar
  9. Bletz, M.C., Goedbloed, D.J., Sanchez, E., Reinhardt, T., Tebbe, C.C., Bhuju, S., Geffers, R., Jarek, M., Vences, M., and Steinfartz, S. (2016). Amphibian gut microbiota shifts differentially in community structure but converges on habitat-specific predicted functions. Nat Commun 7, 13699.PubMedPubMedCentralCrossRefGoogle Scholar
  10. Blooi, M., Martel, A., Haesebrouck, F., Vercammen, F., Bonte, D., and Pasmans, F. (2015a). Treatment of urodelans based on temperature dependent infection dynamics of Batrachochytrium salamandrivorans. Sci Rep 5, 8037.PubMedPubMedCentralCrossRefGoogle Scholar
  11. Blooi, M., Pasmans, F., Rouffaer, L., Haesebrouck, F., Vercammen, F., and Martel, A. (2015b). Successful treatment of Batrachochytrium salamandrivorans infections in salamanders requires synergy between voriconazole, polymyxin E and temperature. Sci Rep 5, 11788.PubMedPubMedCentralCrossRefGoogle Scholar
  12. Blueweiss, L., Fox, H., Kudzma, V., Nakashima, D., Peters, R., and Sams, S. (1978). Relationships between body size and some life history parameters. Oecologia 37, 257–272.PubMedCrossRefGoogle Scholar
  13. Bowden, T.J., Thompson, K.D., Morgan, A.L., Gratacap, R.M.L., and Nikoskelainen, S. (2007). Seasonal variation and the immune response: a fish perspective. Fish Shellfish Immunol 22, 695–706.PubMedCrossRefGoogle Scholar
  14. Brodkin, M.A., Simon, M.P., DeSantis, A.M., and Boyer, K.J. (1992). Response of Rana pipiens to graded doses of the bacterium Pseudomonas aeruginosa. J Herpetol 26, 490.CrossRefGoogle Scholar
  15. Burke, C., Thomas, T., Lewis, M., Steinberg, P., and Kjelleberg, S. (2011). Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J 5, 590–600.PubMedCrossRefGoogle Scholar
  16. Caesar, R., Tremaroli, V., Kovatcheva-Datchary, P., Cani, P.D., and Bäckhed, F. (2015). Crosstalk between gut microbiota and dietary lipids aggravates WAT inflammation through TLR signaling. Cell Metab 22, 658–668.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Calosi, P., Bilton, D.T., and Spicer, J.I. (2008). Thermal tolerance, acclimatory capacity and vulnerability to global climate change. Biol Lett 4, 99–102.PubMedCrossRefGoogle Scholar
  18. Cani, P.D., Amar, J., Iglesias, M.A., Poggi, M., Knauf, C., Bastelica, D., Neyrinck, A.M., Fava, F., Tuohy, K.M., Chabo, C., et al. (2007). Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56, 1761–1772.PubMedCrossRefGoogle Scholar
  19. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7, 335–336.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Careau, V., Biro, P.A., Bonneaud, C., Fokam, E.B., and Herrel, A. (2014). Individual variation in thermal performance curves: swimming burst speed and jumping endurance in wild-caught tropical clawed frogs. Oecologia 175, 471–480.PubMedCrossRefGoogle Scholar
  21. Carr, A.H., Amborski, R.L., Culley, D.D. Jr., and Amborski, G.F. (1976). Aerobic bacteria in the intestinal tracts of bullfrogs (Rana catesbeiana) maintained at low temperatures. Herpetologica 32, 239–244.Google Scholar
  22. Chamaille-Jammes, S., Massot, M., Aragon, P., and Clobert, J. (2006). Global warming and positive fitness response in mountain populations of common lizards Lacerta vivipara. Glob Change Biol 12, 392–402.CrossRefGoogle Scholar
  23. Chang, Y.M., Tseng, W.H., Chen, C.C., Huang, C.H., Chen, Y.F., and Hatch, K.A. (2014). Winter breeding and high tadpole densities may benefit the growth and development of tadpoles in a subtropical lowland treefrog. J Zool 294, 154–160.CrossRefGoogle Scholar
  24. Chang, C.W., Huang, B.H., Lin, S.M., Huang, C.L., and Liao, P.C. (2016). Changes of diet and dominant intestinal microbes in farmland frogs. BMC Microbiol 16, 33.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Chevalier, C., Stojanović, O., Colin, D.J., Suarez-Zamorano, N., Tarallo, V., Veyrat-Durebex, C., Rigo, D., Fabbiano, S., Stevanović, A., Hagemann, S., et al. (2015). Gut microbiota orchestrates energy homeostasis during cold. Cell 163, 1360–1374.PubMedCrossRefGoogle Scholar
  26. Clarke, G., Stilling, R.M., Kennedy, P.J., Stanton, C., Cryan, J.F., and Dinan, T.G. (2014). Minireview: Gut microbiota: the neglected endocrine organ. Mol Endocrinol 28, 1221–1238.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Cooper, R.G., and Kleinschmidt, E.J. (1987). New products: what separates winners from losers? J Prod Innov Manag 4, 169–184.CrossRefGoogle Scholar
  28. Cryan, J.F., and Dinan, T.G. (2012). Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13, 701–712.PubMedCrossRefGoogle Scholar
  29. Daufresne, M., Lengfellner, K., and Sommer, U. (2009). Global warming benefits the small in aquatic ecosystems. Proc Natl Acad Sci USA 106, 12788–12793.PubMedCrossRefGoogle Scholar
  30. Derrien, M., Belzer, C., and de Vos, W.M. (2017). Akkermansia muciniphila and its role in regulating host functions. Microb Pathog 106, 171–181.PubMedCrossRefGoogle Scholar
  31. Desai, A.S., and Singh, R.K. (2009). The effects of water temperature and ration size on growth and body composition of fry of common carp, Cyprinus carpio. J Therm Biol 34, 276–280.CrossRefGoogle Scholar
  32. Deutsch, C.A., Tewksbury, J.J., Huey, R.B., Sheldon, K.S., Ghalambor, C. K., Haak, D.C., and Martin, P.R. (2008). Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci USA 105, 6668–6672.PubMedCrossRefGoogle Scholar
  33. Echaubard, P., Leduc, J., Pauli, B., Chinchar, V.G., Robert, J., and Lesbarrères, D. (2014). Environmental dependency of amphibian-ranavirus genotypic interactions: evolutionary perspectives on infectious diseases. Evol Appl 7, 723–733.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., and Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200.PubMedPubMedCentralCrossRefGoogle Scholar
  35. Everard, A., Belzer, C., Geurts, L., Ouwerkerk, J.P., Druart, C., Bindels, L. B., Guiot, Y., Derrien, M., Muccioli, G.G., Delzenne, N.M., et al. (2013). Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci USA 110, 9066–9071.PubMedCrossRefGoogle Scholar
  36. Geurts, L., Lazarevic, V., Derrien, M., Everard, A., Van Roye, M., Knauf, C., Valet, P., Girard, M., Muccioli, G.G., François, P., et al. (2011). Altered gut microbiota and endocannabinoid system tone in obese and diabetic leptin-resistant mice: impact on apelin regulation in adipose tissue. Front Microbiol 2, 149.PubMedPubMedCentralCrossRefGoogle Scholar
  37. Glorioso, J.C., Amborski, R.L., Amborski, G.F., and Culley, D.D. (1974). Microbiological studies on septicemic bullfrogs (Rana catesbeiana). Am J Vet Res 35, 1241–1245.PubMedGoogle Scholar
  38. Gossling, J., Loesche, W.J., and Nace, G.W. (1982). Response of intestinal flora of laboratory-reared leopard frogs (Rana pipiens) to cold and fasting. Appl Environ Microbiol 44, 67–71.PubMedPubMedCentralGoogle Scholar
  39. Gregor, M.F., and Hotamisligil, G.S. (2011). Inflammatory mechanisms in obesity. Annu Rev Immunol 29, 415–445.PubMedCrossRefGoogle Scholar
  40. Herrel, A., and Bonneaud, C. (2012). Temperature dependence of locomotor performance in the tropical clawed frog, Xenopus tropicalis. J Exp Biol 215, 2465–2470.PubMedCrossRefGoogle Scholar
  41. Hoffmann, I. (2013). Adaptation to climate change—exploring the potential of locally adapted breeds. Animal 7, 346–362.PubMedCrossRefGoogle Scholar
  42. James, R.S., Tallis, J., Herrel, A., and Bonneaud, C. (2012). Warmer is better: thermal sensitivity of both maximal and sustained power output in the iliotibialis muscle isolated from adult Xenopus tropicalis. J Exp Biol 215, 552–558.PubMedCrossRefGoogle Scholar
  43. Kashiwagi, K., Kashiwagi, A., Kurabayashi, A., Hanada, H., Nakajima, K., Okada, M., Takase, M., and Yaoita, Y. (2010). Xenopus tropicalis: an ideal experimental animal in amphibia. Exp Anim 59, 395–405.PubMedCrossRefGoogle Scholar
  44. Khokha, M.K., Chung, C., Bustamante, E.L., Gaw, L.W.K., Trott, K.A., Yeh, J., Lim, N., Lin, J.C.Y., Taverner, N., Amaya, E., et al. (2002). Techniques and probes for the study of Xenopus tropicalis development. Dev Dyn 225, 499–510.PubMedCrossRefGoogle Scholar
  45. Kim, K.A., Gu, W., Lee, I.A., Joh, E.H., and Kim, D.H. (2012). High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PLoS ONE 7, e47713.PubMedPubMedCentralCrossRefGoogle Scholar
  46. King, J.R., Shuter, B.J., and Zimmerman, A.P. (1999). Empirical links between thermal habitat, fish growth, and climate change. Trans Am Fish Soc 128, 656–665.CrossRefGoogle Scholar
  47. Knutie, S.A., Wilkinson, C.L., Kohl, K.D., and Rohr, J.R. (2017a). Early-life disruption of amphibian microbiota decreases later-life resistance to parasites. Nat Commun 8, 86.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Knutie, S.A., Shea, L.A., Kupselaitis, M., Wilkinson, C.L., Kohl, K.D., and Rohr, J.R. (2017b). Early-life diet affects host microbiota and later-life defenses against parasites in frogs. Integr Comp Biol 57, 732–742.PubMedPubMedCentralCrossRefGoogle Scholar
  49. Kohl, K.D., and Yahn, J. (2016). Effects of environmental temperature on the gut microbial communities of tadpoles. Environ Microbiol 18, 1561–1565.PubMedCrossRefGoogle Scholar
  50. Lafferty, K.D. (2009). The ecology of climate change and infectious diseases. Ecology 90, 888–900.PubMedCrossRefGoogle Scholar
  51. Lazzaro, B.P., and Little, T.J. (2009). Immunity in a variable world. Philos Trans R Soc B Biol Sci 364, 15–26.CrossRefGoogle Scholar
  52. Le Morvan, C., Troutaud, D., and Deschaux, P. (1998). Differential effects of temperature on specific and nonspecific immune defences in fish. J Exp Biol 201, 165–168.PubMedGoogle Scholar
  53. Li, W., and Godzik, A. (2006). Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659.PubMedCrossRefGoogle Scholar
  54. Li, H., Li, T., Yao, M., Li, J., Zhang, S., Wirth, S., Cao, W., Lin, Q., and Li, X. (2016). Pika gut may select for rare but diverse environmental bacteria. Front Microbiol 7, 1–7.Google Scholar
  55. Love, M.I., Huber, W., and Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq 2. Genome Biol 15, 550.PubMedPubMedCentralCrossRefGoogle Scholar
  56. Lozupone, C., and Knight, R. (2005). UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71, 8228–8235.PubMedPubMedCentralCrossRefGoogle Scholar
  57. Lu, H., Wu, Z., Xu, W., Yang, J., Chen, Y., and Li, L. (2011). Intestinal microbiota was assessed in cirrhotic patients with hepatitis B virus infection. Microb Ecol 61, 693–703.PubMedCrossRefGoogle Scholar
  58. Lumeng, C.N., and Saltiel, A.R. (2011). Inflammatory links between obesity and metabolic disease. J Clin Invest 121, 2111–2117.PubMedPubMedCentralCrossRefGoogle Scholar
  59. Magoč, T., and Salzberg, S.L. (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963.PubMedPubMedCentralCrossRefGoogle Scholar
  60. Maurice, C.F., Knowles, S.C.L., Ladau, J., Pollard, K.S., Fenton, A., Pedersen, A.B., and Turnbaugh, P.J. (2015). Marked seasonal variation in the wild mouse gut microbiota. ISME J 9, 2423–2434.PubMedPubMedCentralCrossRefGoogle Scholar
  61. McArdle, M.A., Finucane, O.M., Connaughton, R.M., McMorrow, A.M., and Roche, H.M. (2013). Mechanisms of obesity-induced inflammation and insulin resistance: insights into the emerging role of nutritional strategies. Front Endocrinol 4, 52.CrossRefGoogle Scholar
  62. Navas, C.A., Gomes, F.R., and Carvalho, J.E. (2008). Thermal relationships and exercise physiology in anuran amphibians: integration and evolutionary implications. Comp Biochem Physiol Part A Mol Integr Physiol 151, 344–362.CrossRefGoogle Scholar
  63. Ohlberger, J. (2013). Climate warming and ectotherm body size—from individual physiology to community ecology. Funct Ecol 27, 991–1001.CrossRefGoogle Scholar
  64. Qin, N., Yang, F., Li, A., Prifti, E., Chen, Y., Shao, L., Guo, J., Le Chatelier, E., Yao, J., Wu, L., et al. (2014). Alterations of the human gut microbiome in liver cirrhosis. Nature 513, 59–64.PubMedCrossRefGoogle Scholar
  65. Reading, C.J. (2007). Linking global warming to amphibian declines through its effects on female body condition and survivorship. Oecologia 151, 125–131.PubMedCrossRefGoogle Scholar
  66. Ribas, L., Li, M.S., Doddington, B.J., Robert, J., Seidel, J.A., Kroll, J.S., Zimmerman, L.B., Grassly, N.C., Garner, T.W.J., and Fisher, M.C. (2009). Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis. PLoS ONE 4, e8408.PubMedPubMedCentralCrossRefGoogle Scholar
  67. Ridlon, J.M., Alves, J.M., Hylemon, P.B., and Bajaj, J.S. (2013). Cirrhosis, bile acids and gut microbiota. Gut Microb 4, 382–387.CrossRefGoogle Scholar
  68. Rohr, J.R., Raffel, T.R., Romansic, J.M., McCallum, H., and Hudson, P.J. (2008). Evaluating the links between climate, disease spread, and amphibian declines. Proc Natl Acad Sci USA 105, 17436–17441.PubMedCrossRefGoogle Scholar
  69. Shin, N.R., Lee, J.C., Lee, H.Y., Kim, M.S., Whon, T.W., Lee, M.S., and Bae, J.W. (2014). An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut 63, 727–735.PubMedCrossRefGoogle Scholar
  70. Tamaki, H., Wright, C.L., Li, X., Lin, Q., Hwang, C., Wang, S., Thimmapuram, J., Kamagata, Y., and Liu, W.T. (2011). Analysis of 16S rRNA amplicon sequencing options on the Roche/454 next-generation titanium sequencing platform. PLoS ONE 6, e25263–6.PubMedPubMedCentralCrossRefGoogle Scholar
  71. Tryjanowski, P., Sparks, T., Rybacki, M., and Berger, L. (2006). Is body size of the water frog Rana esculenta complex responding to climate change? Naturwissenschaften 93, 110–113.PubMedCrossRefGoogle Scholar
  72. Turnbaugh, P.J., Ridaura, V.K., Faith, J.J., Rey, F.E., Knight, R., and Gordon, J.I. (2009). The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Translational Med 1, 6ra14.CrossRefGoogle Scholar
  73. Warton, D.I., Wright, S.T., and Wang, Y. (2012). Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3, 89–101.CrossRefGoogle Scholar
  74. Wegner, K.M., Kalbe, M., Milinski, M., and Reusch, T.B. (2008). Mortality selection during the 2003 European heat wave in three-spined sticklebacks: effects of parasites and MHC genotype. BMC Evol Biol 8, 124.PubMedPubMedCentralCrossRefGoogle Scholar
  75. Wei, F., Wu, Q., Hu, Y., Huang, G., Nie, Y., and Yan, L. (2019). Conservation metagenomics: a new branch of conservation biology. Sci China Life Sci 62, 168–178.PubMedCrossRefGoogle Scholar
  76. Weng, F.C.H., Yang, Y.J., and Wang, D. (2016). Functional analysis for gut microbes of the brown tree frog (Polypedates megacephalus) in artificial hibernation. BMC Genomics 17, 1024.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Wiebler, J.M., Kohl, K.D., Lee Jr, R.E., and Costanzo, J.P. (2018). Urea hydrolysis by gut bacteria in a hibernating frog: evidence for urea-nitrogen recycling in amphibia. Proc R Soc B 285, 20180241.PubMedCrossRefGoogle Scholar
  78. Zhang, W., Guo, R., Yang, Y., Ding, J., and Zhang, Y. (2016). Long-term effect of heavy-metal pollution on diversity of gastrointestinal microbial community of Bufo raddei. Toxicol Lett 258, 192–197.PubMedCrossRefGoogle Scholar
  79. Zhang, Z., Li, D., Refaey, M.M., Xu, W., Tang, R., and Li, L. (2018). Host age affects the development of southern catfish gut bacterial community divergent from that in the food and rearing water. Front Microbiol 9, 495.PubMedPubMedCentralCrossRefGoogle Scholar
  80. Ziętak, M., Kovatcheva-Datchary, P., Markiewicz, L.H., Ståhlman, M., Kozak, L.P., and Bäckhed, F. (2016). Altered microbiota contributes to reduced diet-induced obesity upon cold exposure. Cell Metab 23, 1216–1223.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Jiaying Li
    • 1
    • 2
    • 3
  • Junpeng Rui
    • 1
    • 2
  • Yulong Li
    • 3
    • 4
  • Na Tang
    • 1
    • 2
  • Songping Zhan
    • 1
    • 2
  • Jianping Jiang
    • 4
    Email author
  • Xiangzhen Li
    • 1
    • 2
    Email author
  1. 1.Key Laboratory of Environmental and Applied MicrobiologyChinese Academy of SciencesChengduChina
  2. 2.Environmental Microbiology Key Laboratory of Sichuan Province, Chengdu Institute of BiologyChinese Academy of SciencesChengduChina
  3. 3.University of Chinese Academy of SciencesBeijingChina
  4. 4.Department of Herpetology, Chengdu Institute of BiologyChinese Academy of SciencesChengduChina

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