[1].The Role of Environmental Stress in Determining Gut Microbiome: Case Study of Two Sympatric Toad-headed Lizards[J].Asian Herpetological Research,2020,11(4):373-380.[doi:10.16373/j.cnki.ahr.200010]
 Yue QI#,Wei ZHAO*,#,et al.The Role of Environmental Stress in Determining Gut Microbiome: Case Study of Two Sympatric Toad-headed Lizards[J].Asian Herpetological Research(AHR),2020,11(4):373-380.[doi:10.16373/j.cnki.ahr.200010]

The Role of Environmental Stress in Determining Gut Microbiome: Case Study of Two Sympatric Toad-headed Lizards()

Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]



The Role of Environmental Stress in Determining Gut Microbiome: Case Study of Two Sympatric Toad-headed Lizards
Yue QI# Wei ZHAO*# Yangyang ZHAO Xiaoning WANG and Chenkai NIU
Gansu Key Laboratory of Biomonitoring and Bioremediation for Environmental Pollution, School of Life Sciences, Lanzhou University, Lanzhou 730000, Gansu, China
gut microbiota environmental factor environmental stress heritable factor toad-headed lizard
The gut microbiota has gained attention because of its importance in facilitating host survival and evolution. However, it is unclear whether gut microbial communities are determined by the host (heritable factor) or environment (environmental factor). In this study, we investigated the gut microbial communities and potential functional signatures of two sympatric species distributed along an elevation gradient, the toad-headed lizards Phrynocephalus axillaris and P. forsythii. Our results indicated that at high elevations, the gut microbial communities of P. axillaris and P. forsythii did not significantly differ, and the phylogenetic relationships of gut microbial communities contradicted their hosts. At low altitudes, the two lizards could be distinguished based on their significantly different gut microbial communities. Compared to low-altitude populations, Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis showed that at higher altitudes, energy metabolism, such as carbohydrate, lipid, and amino acids metabolism were higher in both lizards. While a larger number of pathogenic bacteria were found in the low-altitude population of P. forsythii. This suggests that the convergence of gut microbiota of two lizards at high-altitude stem from environmental factors, as they were exposed to the same environmental stress, whereas the divergence at low-altitude stemmed from heritable factors, as they were exposed to different environmental stresses. These results provide a new perspective regarding whether heritable or environmental factors dominate the gut microbiota during exposure to environmental stress.


Benson A. K., Kelly S. A., Legge R., Ma F., Low S. J., Kim J., Zhang M., Oh P. L., Nehrenberg D., Hua K., Kachman S. D., Moriyama E. N., Walter J,. Peterson D. A., Pomp D. 2010. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. PNAS, 107 (44): 18933–18938
Berg M., Stenuit B., Ho J., Wang A., Parke C, Knight M., Alvarez-Cohen L., Shapira M. 2016. Assembly of the Caenorhabditis elegans gut microbiota from diverse soil microbial environments. ISME Journal, 10(8): 1998–2009
Bermingham E. N., Maclean. P., Thomas D. G., Cave N. J., Young W. 2017. Key bacterial families (Clostridiaceae, Erysipelotrichaceae and Bacteroidaceae) are related to the digestion of protein and energy in dogs. PeerJ, 5: e3019
Bordenstein S. R., Theis K. R. 2015. Host biology in light of the microbiome: ten principles of Holobionts and Hologenomes. PLOS Biol, 13(8): e1002226
Brucker R. M., Bordenstein S. R. 2011. The roles of host evolutionary relationships (genus: Nasonia) and development in structuring microbial communities. Evolution, 66(2): 349–362
Burglin T.R., Mattaj I. W., Newmeyer D. D., Zeller R., De Robertis E. M. 1987. Cloning of nucleoplasmin from Xenopus laevis oocytes and analysis of its developmental expression. Genes Dev, 1(1): 97–107
Caporaso J. G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F. D., Costello E. K., Fierer N., Pe?a A. G., Goodrich J. K., Gordon J. I., Huttley G. A., Kelley S. T., Knights D., Koenig J. E., Ley R. E., Lozupone C. A., McDonald D., Muegge B. D., Pirrung M., Reeder J., Sevinsky J. R., Turnbaugh P. J., Walters W. A., Widmann J., Yatsunenko T., Zaneveld J., Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods, 7(6): 335–336
Carmody R. N., Gerber G. K., Luevano J. M., Gatti D. M., Somes L., Svenson K. L., Turnbaugh P. J. 2015. Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe, 17(1): 72–84
Choi M. S., Kim Y. J., Kwon E. Y., Ryoo J. Y., Kim S. R., Jung U. J. 2015. High-fat diet decreases energy expenditure and expression of genes controlling lipid metabolism, mitochondrial function and skeletal system development in the adipose tissue, along with increased expression of extracellular matrix remodelling- and inflammation-related genes. Brit J Nutr, 113(6): 867–877
Clarke K. R. 1993. Non-parametric multivariate analysis of changes in community structure. Austral J Ecol, 18(1): 117–143
Clark M. A., Moran N. A., Baumann P., Wernegreen J. J. 2000. Cospeciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution, 54(2): 517–525
Colston J. T. 2017. Gut microbiome transmission in lizards. Mol Ecol, 26(4): 972–974
Dai Z. L., Wu G., Zhu W. Y. 2011. Amino acid metabolism in intestinal bacteria: links between gut ecology and host health. Front Biosci, 16(1): 1768–1786
Han J. M., Guo R. H., Li J. Q., Guan C., Chen Y., Zhao W. 2016. Organ Mass Variation in a toad headed Lizard Phrynocephalus vlangalii in response to hypoxia and low temperature in the Qinghai-Tibet plateau, China. PLoS One, 11(9): e0162572
Kikuchi Y., Hayatsu M., Hosokawa T., Nagayama A., Tago K., Fukatsu T. 2012. Symbiont-mediated insecticide resistance. PNAS, 109(22): 8618–8622
Kocan K. M., Fuente J. D. L., Blouin E. F., Garcia-Garcia J. C. 2004. Anaplasma marginale (Rickettsiales: Anaplasmataceae): recent advances in defining host-pathogen adaptations of a tick-borne rickettsia. Parasitology, 129(7): 285–300
Langille M. G., Zaneveld J., Caporaso J. G., McDonald D., Knights D., Reyes J. A., Clemente J. C., Burkepile D. E., Vega-Thurber R. L., Knight R., Beiko R. G., Huttenhower C. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol, 31(9): 814–821
McFall-Ngai M., Hadfield M. G., Bosch T. C., Carey H. V., Domazet-Lo?o T., Douglas A. E., Dubilier N., Eberl G., Fukami T., Gilbert S. F., Hentschel U., King N., Kjelleberg S., Knoll A. H., Kremer N., Mazmanian S. K., Metcalf J. L., Nealson K., Pierce N. E., Rawls J. F., Reid A., Ruby E. G., Rumpho M., Sanders J. G., Tautz D., Wernegreen J. J. 2012. Animals in a bacterial world, a new imperative for the life sciences. PNAS, 110(9): 3229–3236
Moeller A. H., Peeters M., Ndjango J. B., Li Y., Hahn B. H., Ochman, H. 2013. Sympatric chimpanzees and gorillas harbor convergent gut microbial communities. Genome Res, 23(10): 1715–1720
Parks D. H., Tyson G. W., Hugenholtz P., Beiko R. G. 2014. STAMP: Statistical analysis of taxonomic and functional profiles. Bioinformatics, 30(21): 3123–3124
Qi Y., Zhao W., Huang Y. J., Wang X. N., Zhao Y. Y. 2019. Correlation between climatic factors and genetic diversity of Phrynocephalus forsythii. Asian Herpeto Res, 10(4): 270–275
Roeselers G., Mittge E. K., Stephens W. Z., Parichy D. M., Cavanaugh C. M., Guillemin K., Rawls J. F. 2011. Evidence for a core gut microbiota in the zebrafish. ISME J, 5(10): 1595–1608
Rothschild D., Weissbrod O., Barkan E., Kurilshikov A., Korem T., Zeevi D., Costea P. I., Godneva A., Kalka I. N., Bar N., Shilo S., Lador D., Vila A. V., Zmora N., Pevsner-Fischer M., Israeli D., Kosower N., Malka G., Wolf B. C., Avnit-Sagi T., Lotan-Pompan M., Weinberger A., Halpern Z., Carmi S., Fu J., Wijmenga C., Zhernakova A., Elinav E., Segal E. 2018. Environment dominates over host genetics in shaping human gut microbiota. Nature, 555(7695): 210–215
Shapira M. 2016. Gut Microbiotas and host evolution: Scaling up symbiosis. Trends Ecol Evol, 31(7): 539–549
Sinervo B., Miles D. B., Wu Y. Y., R. Méndez-De La Cruz., Kirchhof S. 2018. Climate change, thermal niches, extinction risk and maternal-effect rescue of toad-headed lizards, Phrynocephalus, in thermal extremes of the Arabian peninsula to the Tibetan Plateau. Integr Zool, 13(4): 450–470
Song S. J., Sanders J. G., Baldassarre D. T., Chaves J. A., Johnson N. S., Piaggio A. J.,, Stuckey M. J., Novakova E., Metcalf J. L., Chomel B. B., AguilarSetien A., Knight R., McKenzie V. J. 2019. Is there convergence of gut microbes in blood-feeding vertebrates? Philos T R Soc B, 374(1777): 20180249
Spanogiannopoulos P., Bess E. N., Carmody R. N., Turnbaugh P. J. 2016. The microbial pharmacists within us: A metagenomic view of xenobiotic metabolism. Nat Rev Microbiol, 14(5): 273–287
Spencer M. D., Hamp T. J., Reid R. W., Fischer L. M., Zeisel S. H., Fodor A. A. 2011. Association between composition of the human gastrointestinal microbiome and development of fatty liver with choline deficiency. Gastroenterology, 140(3): 976–986
Sun L. J., Ma L. J., Ma Y. B., Zhang F. M., Zhao C. H., Nie Y. 2018. Insights into the role of gut microbiota in obesity: Pathogenesis, mechanisms, and therapeutic perspectives. Protein Cell, 9(5): 397–403
Suzuki T. A., Phifer-Rixey M., Mack K. L., Sheehan M. J., Lin D., Bi K., Nachman M. W. 2019. Host genetic determinants of the gut microbiota of wild mice. Mol Ecol, 28(1): 3197–3207
Tang X., Xin Y., Wang H., Li W., Zhang Y., Liang S., He J., Wang N., Ma M., Chen Q. 2013. Metabolic characteristics and response to high altitude in Phrynocephalus erythrurus (Lacertilia: Agamidae), a lizard dwell at altitudes higher than any other living lizards in the world. Plos One, 8(8): e71976
Vazquez-Baeza Y., Pirrung M., Gonzalez A., Knight R. 2013. EMPeror: A tool for visualizing high-throughput microbial community data. Gigascience, 2(1): 16–20
Wang Q., Garrity G. M., Tiedje J. M., Cole J. R. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb, 73(16): 5261–5267
Wu D. Y., Hugenholtz P., Mavromatis K., Pukall R., Dalin E., Ivanova N. N., Kunin V., Goodwin L., Wu M., Tindall B. J., Hooper S. D., Pati A., Lykidis A., Spring S., Anderson I. J., D’haeseleer P., Zemla A., Singer M., Lapidus A., Nolan M., Copeland A., Han C., Chen F., Cheng J. F., Lucas S., Kerfeld C., Lang E., Gronow S., Chain P., Bruce D., Rubin E. M., Kyrpides N. C., Klenk H. P., Eisen J. A. 2009. A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature, 462(7276): 24–31
Yan H., Caporaso J. G., Jiang X. T., Sheng H. F., Huse S. M., Rideout J. R., Edgar R. C., Kopylova E., Walters W. A., Knight R., Zhou H. W. 2015. Stability of operational taxonomic units: An important but neglected property for analyzing microbial diversity. Microbiome, 3: 20–30
Yang W. Z., Qi Y., Fu J. Z. 2014a. Exploring the genetic basis of adaptation to high elevations in reptiles: A comparative transcriptome analysis of two toad-headed agamas (genus Phrynocephalus). PLoS One, 9(11): e112218
Yang Y. X., Dai Z. L., Zhu W. Y. 2014b. Important impacts of intestinal bacteria on utilization of dietary amino acids in pigs. Amino Acids, 46(11): 2489–2501
Zhang W. Y., Li N., Tang X. L., Liu N. F., Zhao W. 2018. Changes in intestinal microbiota across an altitudinal gradient in the lizard Phrynocephalus vlangalii. Ecol Evol, 8(9): 4695–4703

更新日期/Last Update: 2020-12-25