高原鼠兔肠道微生物中丰富及稀有类群的季节性特征

范超; 张良志; 付海波; 刘传发; 李文靖; 张贺; 唐显江; 程琪; 沈文娟; 张堰铭

doi:10.16829/j.slxb.150540

兽类学报 >

2021 , Vol. 41 >Issue 6: 617 - 630

DOI: https://doi.org/10.16829/j.slxb.150540

研究论文

高原鼠兔肠道微生物中丰富及稀有类群的季节性特征

范超 ,
张良志 ,
付海波 ,
刘传发 ,
李文靖 ,
张贺 ,
唐显江 ,
程琪 ,
沈文娟 ,
张堰铭

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1 中国科学院西北高原生物研究所, 中国科学院高原生物适应与进化重点实验室, 西宁 810001;
2 中国科学院大学, 北京 100049;
3 青海大学青海省畜牧兽医科学院, 西宁 810016

范超(1993-),男,博士研究生,主要从事分子生态学研究.

收稿日期: 2021-03-15

修回日期: 2021-05-24

网络出版日期: 2021-05-24

基金资助

国家自然科学基金（31670394）；第二次青藏高原科考研究计划（2019QZKK0501）；青海省科技厅重大专项“三江源国家公园动物基因组计划”

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Seasonality of abundant and rare taxa in gut microbiota of plateau pikas

FAN Chao ,
ZHANG Liangzhi ,
FU Haibo ,
LIU Chuanfa ,
LI Wenjing ,
ZHANG He ,
TANG Xianjiang ,
CHENG Qi ,
SHEN Wenjuan ,
ZHANG Yanming

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1 Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810001, China;
2 University of Chinese Academy of Sciences, Beijing 100049, China;
3 Academy of Animal Husbandry and Veterinary Medicine, Qinghai University, Xining 810016, China

Received date: 2021-03-15

Revised date: 2021-05-24

Online published: 2021-05-24

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摘要

气候及食物是驱动植食性小哺乳动物肠道菌群产生季节性变化的重要因素。然而，此类研究很少涉及肠道丰富及稀有微生物类群。本文以高原鼠兔（Ochotona curzoniae）为对象，通过16S rRNA基因测序和分析，探讨丰富及稀有肠道微生物类群的结构组成、多样性指数及功能在春、夏、秋、冬四季的变化特征。结果显示，丰富类群对菌群主要门和功能的季节性变异贡献大于稀有类群，稀有类群对菌群OTU和alpha多样性的变异贡献大于丰富类群。丰富类群和稀有类群的香农指数均在冬季显著高于其他季节；丰富类群的ACE指数在秋季显著低于其他季节，而稀有类群的ACE指数则在冬季显著高于春季和夏季。丰富类群中拟杆菌门（Bacteroidetes）的相对丰度在冬季和秋季显著高于春季和夏季，但在稀有类群中，夏季和秋季的相对丰度显著高于冬季和春季。丰富类群中氨基酸代谢通路的相对丰度在冬季显著高于春季和夏季，而在稀有类群中，其相对丰度在春季显著高于夏季和秋季。气温、降水量和植被中的营养物质与肠道菌群中丰富类群和稀有类群的变化均显著相关，环境变量对丰富类群和稀有类群变化的总解释率分别为18%（气温：3%；降水：4%；植被营养成分：10%；联合：1%）和9%（气温：1%；降水：2%；植被营养成分：5%；联合：1%）。以上结果表明肠道微生物中的丰富和稀有类群具有不同的分布模式和季节性特征，二者对整体菌群变异的贡献存在差异，环境因素更多地影响丰富类群，反映了肠道微生物不同类群对季节变化响应的非一致性。本研究增进了我们对哺乳动物肠道菌群季节性变化过程及环境适应性的认识。

关键词： 肠道微生物; 16S rRNA基因; 丰富和稀有类群; 季节性特征; 高原鼠兔

本文引用格式

范超 , 张良志 , 付海波 , 刘传发 , 李文靖 , 张贺 , 唐显江 , 程琪 , 沈文娟 , 张堰铭 . 高原鼠兔肠道微生物中丰富及稀有类群的季节性特征[J]. 兽类学报, 2021 , 41(6) : 617 -630 . DOI: 10.16829/j.slxb.150540

Abstract

Climate and diet are important factors driving seasonal changes in gut microbiota of small herbivorous mammals. However, most previous studies rarely addressed abundant and rare taxa in gut microbiota. Here, we used plateau pika (Ochotona curzoniae) as a model and conducted 16S rRNA gene-based large-scale structural profiling to explore the seasonal differences (spring, summer, autumn, and winter) in microbial composition, diversity, and function in abundant and rare taxa. The results showed that the Shannon index of abundant and rare taxa was significantly higher in winter than in other seasons. However, the ACE index of abundant taxa was significantly lower in autumn than in other seasons while that of rare taxa was significantly higher in winter than in spring and summer. For the abundant taxa, the relative abundance of Bacteroidetes in winter and autumn was significantly higher than that in spring and summer, while for the rare taxa, the relative abundance of Bacteroidetes in summer and autumn was significantly higher than that in winter and spring. The relative abundance of the amino acid metabolism pathway in abundant taxa was significantly higher in winter than that in spring and summer, while the relative abundance of this pathway in rare taxa was significantly higher in spring than that in summer and autumn. Air temperature, precipitation, and vegetative nutrition were significantly associated with variations in the microbial composition of both abundant and rare taxa. The total explanation proportions of environmental variables to the changes of abundant and rare taxa were 18% (air temperature:3%; precipitation:4%; vegetative nutrition:10%; combined:1%) and 9% (air temperature:1%; precipitation:2%; vegetative nutrition:5%; combined:1%), respectively. The results indicate that abundant and rare taxa of gut microorganisms have different distribution patterns, seasonal characteristics, and contributions to the entire microbial variation. The abundant taxa were more strongly influenced by environmental variables, reflecting the inconsistency in responses of different gut microbial taxa to seasonal changes. This study promotes our understanding of seasonal processes and environmental adaptability of animal's gut microbiota.

Key words： Gut microbiota; 16S rRNA gene; Abundant and rare taxa; Seasonality; Plateau pika (Ochotona curzoniae)

参考文献

Amato K R, Leigh S R, Kent A, Mackie R I, Yeoman C J, Stumpf R M, Wilson B A, Nelson K E, White B A, Garber P A.2015.The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra).Microbial Ecology, 69:434-443.
Bestion E, Jacob S, Zinger L, Di Gesu L, Richard M, White J, Cote J.2017.Climate warming reduces gut microbiota diversity in a vertebrate ectotherm.Naturea Ecology and Evolution, 1:161.
Cheaib B, Seghouani H, Llewellyn M, Vandal-Lenghan K, Mercier PL, Derome N.2021.The yellow perch (Perca flavescens) microbiome revealed resistance to colonisation mostly associated with neutralism driven by rare taxa under cadmium disturbance.Animal Microbiome, 3:3.
Chen S, Zhou Y, Chen Y, Gu J.2018.fastp:an ultra-fast all-in-one FASTQ preprocessor.Bioinformatics, 34:i884-890.https://doi.org/10.1093/bioinformatics/bty560.
Cottrell M T, David K L.2003.Contribution of major bacterial groups to bacterial biomass production (thymidine and leucine incorporation) in the Delaware estuary.Limnology and Oceanography, 48:168-178.https://doi.org/10.4319/lo.2003.48.1.0168.
DeLong E F.2014.Alien invasions and gut"island biogeograph".Cell, 159:233-235.
Edgar R C.2013.UPARSE:highly accurate OTU sequences from microbial amplicon reads.Nature Methods, 10:996-998.https://doi.org/10.1038/nmeth.2604.
Fan C, Zhang L, Fu H, Liu C, Li W, Cheng Q, Zhang H, Jia S, Zhang Y.2020.Enterotypes of the gut microbial community and their response to plant secondary compounds in plateau pikas.Microorganisms, 8:1311.
Guo J, Yuan Z, Zhang W, Zhang M.2020.The microbial composition and community diversity of red deer (Cervus elaphus xanthopygus) in winter in Chifeng region of Inner Mongolia.Chinese Journal of Wildlife, 41:261-271.(in Chinese).
Hausmann B, Knorr K H, Schreck K, Tringe S G, Glavina Del Rio T, Loy A, Pester M.2016.Consortia of low-abundance bacteria drive sulfate reduction-dependent degradation of fermentation products in peat soil microcosms.The ISME Journal, 10:2365-2375.https://doi.org/10.1038/ismej.2016.42.
Ji M, Kong W, Stegen J, Yue L, Wang F, Dong X, Cowan D A, Ferrari B C.2020.Distinct assembly mechanisms underlie similar biogeographical patterns of rare and abundant bacteria in Tibetan Plateau grassland soils.Environmental Microbiology, 22:2261-2272.https://doi.org/10.1111/1462-2920.14993.
Jia S.2012.Change trend and correlation analysis of temperature and precipitation in Gangcha county during 1961-2006.Journal of Anhui Agricultural Sciences, 40:231-232.(in Chinese).
Jia X, Dini-Andreote F, Falcão Salles J.2018.Community assembly processes of the microbial rare biosphere.Trends in Microbiology, 26:738-747.https://doi.org/10.1016/j.tim.2018.02.011.
Jiao S, Lu Y.2020.Abundant fungi adapt to broader environmental gradients than rare fungi in agricultural fields.Global Change Biology, 26:4506-4520.https://doi.org/10.1111/gcb.15130.
Jiao S, Luo Y, Lu M, Xiao X, Lin Y, Chen W, Wei G.2017.Distinct succession patterns of abundant and rare bacteria in temporal microcosms with pollutants.Environmental Pollution, 225:497-505.https://doi.org/10.1016/j.envpol.2017.03.015.
Jiao S, Wang J, Wei G, Chen W, Lu Y.2019.Dominant role of abundant rather than rare bacterial taxa in maintaining agro-soil microbiomes under environmental disturbances.Chemosphere, 235:248-259.
Kalamees R, Zobel M.2002.The role of the seed bank in gap regeneration in a calcareous grassland community.Ecology, 83:1017-1025.https://doi.org/10.2307/3071910.
Karlsen C, Ottem K F, Brevik Ø J, Davey M, Sørum H, Winther-Larsen H C.2017.The environmental and host-associated bacterial microbiota of Arctic seawater-farmed Atlantic salmon with ulcerative disorders.Journal of Fish Diseases, 40:1645-1663.https://doi.org/10.1111/jfd.12632.
Langille M G I, 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.Nature Biotechnology, 31:814-821.https://doi.org/10.1038/nbt.2676.
Lennon J T, Jones S E.2011.Microbial seed banks:the ecological and evolutionary implications of dormancy.Nature Reviews Microbiology, 9:119-130.https://doi.org/10.1038/nrmicro2504.
Li G, Yin B, Li J, Wang J, Wei W, Bolnick D I, Wan X, Zhu B, Zhang Z.2020.Host-microbiota interaction helps to explain the bottom-up effects of climate change on a small rodent species.The ISME Journal, 14:1795-1808.https://doi.org/10.1038/s41396-020-0646-y.
Li H, Qu J, Li T, Li J, Lin Q, Li X.2016.Pika population density is associated with the composition and diversity of gut microbiota.Front Microbiology, 7:758.
Li H, Zhou R, Zhu J, Huang X, Qu J.2019.Environmental filtering increases with elevation for the assembly of gut microbiota in wild pikas.Microbial Biotechnology, 12:976-992.https://doi.org/10.1111/1751-7915.13450.
Liang Y, Xiao X, Nuccio E E, Yuan M, Zhang N, Xue K, Cohan F M, Zhou J, Sun B.2020.Differentiation strategies of soil rare and abundant microbial taxa in response to changing climatic regimes.Environmental Microbiology, 22:1327-1340.https://doi.org/10.1111/1462-2920.14945.
Liu L, Yang J, Yu Z, Wilkinson D M.2015.The biogeography of abundant and rare bacterioplankton in the lakes and reservoirs of China.The ISME Journal, 9:2068-2077.https://doi.org/10.1038/ismej.2015.29.
Maurice C F, Knowles S C L, Ladau J, Pollard K S, Fenton A, Pedersen A B, Turnbaugh P J.2015.Marked seasonal variation in the wild mouse gut microbiota.The ISME Journal, 9:2423-2434.https://doi.org/10.1038/ismej.2015.53.
McDonald D, Price M N, Goodrich J, Nawrocki E P, DeSantis T Z, Probst A, Andersen G L, Knight R, Hugenholtz P.2012.An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea.The ISME Journal, 6:610-618.https://doi.org/10.1038/ismej.2011.139.
Mo Y, Zhang W, Yang J, Lin Y, Yu Z, Lin S.2018.Biogeographic patterns of abundant and rare bacterioplankton in three subtropical bays resulting from selective and neutral processes.The ISME Journal, 12:2198-2210.https://doi.org/10.1038/s41396-018-0153-6.
Orkin J D, Campos F A, Myers M S, Cheves Hernandez S E, Guadamuz A, Melin A D.2019.Seasonality of the gut microbiota of free-ranging white-faced capuchins in a tropical dry forest.The ISME Journal, 13:183-196.https://doi.org/10.1038/s41396-018-0256-0.
Qu J, Liu M, Yang M, Zhang Y.2012.Reproduction of plateau pika(Ochotona curzoniae) on the Qinghai-Tibetan Plateau.European Journal of Wildlife Research, 58:269-277.https://doi.org/10.1007/s10344-011-0574-2.
Scheckenbach F, Hausmann K, Wylezich C, Weitere M, Arndt H.2010.Large-scale patterns in biodiversity of microbial eukaryotes from the abyssal sea floor.Proceedings of the National Academy of Sciences of the United States of America, 107:115-120.https://doi.org/10.1073/pnas.0908816106.
Siles J A, Margesin R.2017.Seasonal soil microbial responses are limited to changes in functionality at two Alpine forest sites differing in altitude and vegetation.Scientific Reports, 7:2204.https://doi.org/10.1038/s41598-017-02363-2.
Shin N R, Whon T W, Bae J W.2015.Proteobacteria:microbial signature of dysbiosis in gut microbiota.Trends in Biotechnology, 33:496-503.https://doi.org/10.1016/j.tibtech.2015.06.011.
Sloan W T, Lunn M, Woodcock S, Head I M, Nee S, Curtis T P.2006.Quantifying the roles of immigration and chance in shaping prokaryote community structure.Environmental Microbiology, 8:732-740.
Smith A T, Badingqiuying, Wilson M C, Hogan B W.2019.Functional-trait ecology of the plateau pika Ochotona curzoniae in the Qinghai-Tibetan Plateau ecosystem.Integrative Zoology, 14:87-103.https://doi.org/10.1111/1749-4877.12300.
Tan C, Li H, Qu J.2019.Comparison of gut microbial diversity between wild and laboratory-reared plateau pika (Ochotona curzoniae).Pratacult Science, 36:531-539.(in Chinese)
Tan L, Zhao S, Zhu W, Wu L, Li J, Shen M, Lei L, Chen X, Peng C.2018.The Akkermansia muciniphila is a gut microbiota signature in psoriasis.Experimental Dermatology, 27:144-149.https://doi.org/10.1111/exd.13463.
Tong Q, Hu Z F, Du X P, Bie J, Wang H B.2020.Effects of seasonal hibernation on the similarities between the skin microbiota and gut microbiota of an Amphibian (Rana dybowskii).Microbial Ecology, 79:898-909.https://doi.org/10.1007/s00248-019-01466-9.
Wang J, Zhang Y, Wang D.2006.Seasonal thermogenesis and body mass regulation in plateau pikas (Ochotona curzoniae).Oecologia, 149:373-382.https://doi.org/10.1007/s00442-006-0469-1.
Wang Y, Hatt J K, Tsementzi D, Rodriguez-R L M, Ruiz-Pérez C A, Weigand M R, Kizer H, Maresca G, Krishnan R, Poretsky R, Spain J C, Konstantinidis K T.2017.Quantifying the importance of the rare biosphere for microbial community response to organic pollutants in a freshwater ecosystem.Applied and Environmental Microbiology, 83:e03321-16.
Wei G, Li M, Li F, Li H, Gao Z.2016.Distinct distribution patterns of prokaryotes between sediment and water in the Yellow River estuary.Applied Microbiology and Biotechnology, 100:9683-9697.https://doi.org/10.1007/s00253-016-7802-3.
Yan Q, Li J, Yu Y, Wang J, He Z, Van Nostrand J D, Kempher M L, Wu L, Wang Y, Liao L, Li X, Wu S, Ni J, Wang C, Zhou J.2016.Environmental filtering decreases with fish development for the assembly of gut microbiota.Environmental Microbiology, 18:4739-4754.https://doi.org/10.1111/1462-2920.13365.
Zhao J, Xing S, Ma Y.2012.Characteristics of soil moisture for different types of vegetation in Gangcha County.Bulletin of Soil and Water Conservation, 32:14-18.(in Chinese)
Zhu W, Zhang D, Jiang N, Zheng Z.2019.Spatiotemporal variations of the start of thermal growing season for grassland on the Qinghai-Tibetan Plateau during 1961-2014.Internayional Journal of Biometeorology, 63:639-647.https://doi.org/10.1007/s00484-017-1426-x.
Zu J, Zhang Y, Huang K, Liu Y, Chen N, Cong N.2018.Biological and climate factors co-regulated spatial-temporal dynamics of vegetation autumn phenology on the Tibetan Plateau.International Journal of Applied Earth Observation and Geoinformation, 69:198-205.
郭金昊, 袁子奥, 张玮琪, 张明海.2020.内蒙古赤峰地区东北马鹿 (Cervus elaphus xanthopygus)冬季肠道微生物多样性研究.野生动物学报, 41:261-271.
贾顺斌.2012.刚察县 1961~2006年气温与降水的变化趋势及相关性分析.安徽农业科学, 40:231-232.
谭春桃, 李欢, 曲家鹏.2019.野生和室内饲养高原鼠兔肠道菌群多样性的比较.草业科学, 36:531-539.
赵景波, 邢闪, 马延东.2012.刚察县不同植被类型的土壤水分特征研究.水土保持通报, 32:14-18.

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