越冬动物肠道微生物多样性及功能研究进展

doi:10.17520/biods.2023407

生物多样性 ›› 2024, Vol. 32 ›› Issue (3): 23407. DOI: 10.17520/biods.2023407

越冬动物肠道微生物多样性及功能研究进展

郝操¹, 吴东辉²^,³, 莫凌梓¹, 徐国良¹^,^*()

1.广州大学地理科学与遥感学院广东省农村水环境面源污染综合治理工程技术研究中心, 广州 510006
2.东北师范大学环境学院国家环境保护湿地生态与植被恢复重点实验室, 长春 130117
3.中国科学院东北地理与农业生态研究所湿地生态与环境重点实验室, 长春 130102

收稿日期:2023-10-24 接受日期:2024-01-02 出版日期:2024-03-20 发布日期:2024-01-16
通讯作者: *E-mail: xugl@gzhu.edu.cn
基金资助:
国家自然科学基金(42071061)

A review on gut microbial diversity and function of overwintering animals

Cao Hao¹, Donghui Wu²^,³, Lingzi Mo¹, Guoliang Xu¹^,^*()

1 Rural Non-Point Source Pollution Comprehensive Management Technology Center of Guangdong Province, School of Geography and Remote Sensing, Guangzhou University, Guangzhou 510006
2 State Environmental Protection Key Laboratory of Wetland Ecology and Vegetation Restoration, School of Environment, Northeast Normal University, Changchun 130117
3 Key Laboratory of Wetland Ecology and Environment, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102

Received:2023-10-24 Accepted:2024-01-02 Online:2024-03-20 Published:2024-01-16
Contact: *E-mail: xugl@gzhu.edu.cn

摘要/Abstract

摘要：

越冬是全球温带和寒带地区动物生活史和演化过程的重要阶段, 顺利越冬对于动物种群的繁衍与维持至关重要。肠道微生物与宿主长期共同进化并形成复杂的共生关系, 在动物生长发育、健康调控及恶劣环境适应等方面发挥着重要作用。越冬动物不仅在形态、生理和行为方面发生适应性变化, 其肠道微生物也发生改变, 这对宿主适应低温不可或缺。近些年越冬动物肠道微生物工作日渐受到重视, 鉴于肠道微生物的重要意义, 本文总结和评述了4个方面内容: (1)越冬动物肠道微生物领域的研究现状。该领域发文量近年来增长快速, 冬眠动物肠道微生物研究最多且更为深入。肠道微生物多样性、影响因素和群落构建机制以及肠道微生物对动物越冬的作用机制是该领域的研究热点; (2)越冬动物肠道微生物群落多样性、组成及其功能基因的变化。冬季动物肠道细菌群落以拟杆菌门、厚壁菌门和变形菌门为主, 且多样性较夏季更低。冬眠动物肠道细菌群落的功能基因以脂肪代谢为主; (3)影响冬季动物肠道微生物群落的主要因素。肠道微生物群落与越冬宿主肠道形态和生理、物种类别、食性、越冬策略及外界环境时空和气候变化密切联系; (4)肠道微生物在动物越冬方面发挥的重要功能。肠道微生物参与宿主营养获取和能量代谢、调节宿主产热、影响宿主抗冻性及免疫力。本研究可增加人们对非生长季动物肠道微生物多样性维持及其生态功能的认识, 并帮助深入思考肠道微生物及其与宿主互作机制在调控动物适应环境变化方面的潜在影响。

关键词: 冬眠, 滞育, 肠道菌群, 宿主-微生物互作, 冬季生物多样性, 冷适应

Abstract

Background & Aim: Overwintering is an important stage in the life history and evolution of animals in temperate and cold regions of the world, and successful overwintering is crucial for the reproduction and maintenance of animal populations. Gut microbiota and hosts have co-evolved and formed complex symbiotic relationships that play important roles in animal growth and development, health regulation and adaptation to harsh environments. Overwintering animals undergo not only adaptive changes in morphology, physiology and behavior, but also changes in their gut microbiota, which are essential for host adaptation to low temperatures. In recent years, the work on the gut microbiota of overwintering animals has received increasing attention.
Review results: (1) We summarized the current progress in studies of the gut microbiota of overwintering animals. The number of publications in this field has increased rapidly in recent years, and gut microbiota of hibernating animals has been studied most intensively. Gut microbial diversity, influencing factors, community assembly, and the mechanism of gut microbiota on overwintering animals are the research hotspots. (2) We analyzed the changes in diversity, composition and functional genes of the gut microbial community in overwintering animals. Bacteroidetes, Firmicutes and Proteobacteria dominate the gut bacterial communities in winter, and their diversity is lower than that in summer. The functional genes of the gut bacterial community in hibernating animals are mainly related to lipid metabolism. (3) We summarized the main factors influencing the gut microbial community of overwintering animals. The gut microbial community is closely related to the gut morphology and physiology, species identification, diet, overwintering strategy, spatio-temporal and climatic changes. (4) We discussed the important functions of the gut microbiota during overwintering. Gut microbiota are involved in nutrition acquisition and energy metabolism, heat production, and influenced host cold tolerance and immunity of the hosts.
Suggestions & Perspectives: This review can enhance our understanding of the maintenance of gut microbial diversity and its ecological function in the non-growing season, and help to understand the potential impact of gut microbiota and their host interaction mechanisms on the regulation of animal adaptation to environmental changes.

Key words: hibernation, diapause, gut microbiota, host-microbe interaction, winter biodiversity, cold adaptation

郝操, 吴东辉, 莫凌梓, 徐国良 (2024) 越冬动物肠道微生物多样性及功能研究进展. 生物多样性, 32, 23407. DOI: 10.17520/biods.2023407.

Cao Hao, Donghui Wu, Lingzi Mo, Guoliang Xu (2024) A review on gut microbial diversity and function of overwintering animals. Biodiversity Science, 32, 23407. DOI: 10.17520/biods.2023407.

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链接本文: https://www.biodiversity-science.net/CN/10.17520/biods.2023407

https://www.biodiversity-science.net/CN/Y2024/V32/I3/23407

图/表 2

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宿主 Host		越冬策略 Overwintering strategy	越冬肠道细菌多样性 Gut bacterial diversity in winter	越冬肠道优势细菌门 Gut dominating bacterial phylum in winter	越冬肠道主要功能代谢 Gut main metabolic function in winter	参考文献 References
纲名 Class	种名 Species	越冬策略 Overwintering strategy	越冬肠道细菌多样性 Gut bacterial diversity in winter	越冬肠道优势细菌门 Gut dominating bacterial phylum in winter	越冬肠道主要功能代谢 Gut main metabolic function in winter	参考文献 References
哺乳纲 Mammalia	野牦牛 Bos mutus	活跃 Active	Chao 1丰富度指数↑ Chao 1 index ↑	拟杆菌门、厚壁菌门 Bacteroidetes, Firmicutes	脂肪细胞因子信号通路↑、脂肪酸降解↑ Adipocytokine signalling pathway ↑, fatty acid degradation ↑	Fu et al, 2021
哺乳纲 Mammalia	马铁菊头蝠 Rhinolophus ferrumequinum	冬眠 Hibernate	Chao 1丰富度指数↓、Shannon多样性指数↓ Chao 1 index ↓, Shannon index ↓	变形菌门、厚壁菌门↓ Proteobacteria, Firmicutes ↓	碳水化合物代谢↓、脂肪代谢↑ Carbohydrate metabolism ↓, lipid metabolism ↑	Xiao et al, 2019
鸟纲 Aves	艾草松鸡 Centrocercus urophasianus	活跃 Active	物种数↓、Shannon多样性指数↓ Observed species ↓, Shannon index ↓	欧陆森氏菌属↑, 巴斯德菌科↑ Olsenella ↑, Pasteurellaceae ↑	-	Drovetski et al, 2019
鸟纲 Aves	白额雁 Anser albifrons	活跃 Active	-	厚壁菌门、变形菌门、放线菌门 Firmicutes, Proteobacteria, Actinobacteri	碳水化合物代谢、氨基酸代谢 Carbohydrate metabolism, amino acid metabolism	Yang et al, 2016
两栖纲 Amphibia	东北林蛙 Rana dybowskii	冬眠 Hibernate	物种数↓、Chao 1丰富度指数↓、Shannon多样性指数↓ Observed species ↓, Chao 1 index ↓, Shannon index ↓	厚壁菌门↓、弯曲菌门↑ Firmicutes ↓, Campylobacterota ↑	-	Tong et al, 2023
两栖纲 Amphibia	扬子鳄 Alligator sinensis	冬眠 Hibernate	物种数↑、Chao 1丰富度指数↑、Shannon多样性指数 Observed species ↑, Chao 1 index ↑, Shannon index	变形菌门、拟杆菌门↑ Proteobacteria, Bacteroidetes ↑	粘蛋白寡糖降解酶↑ Mucin oligosaccharide- degrading enzymes ↑	Tang et al, 2019
昆虫纲 Insecta	西方蜜蜂 Apis mellifera	滞育 Diapause	Chao 1丰富度指数↓、Shannon多样性指数↓ Chao 1 index ↓, Shannon index ↓	根瘤菌科↑、肠杆菌科↓ Rhizobiaceae ↑, Enterobacteriaceae↓	-	Bleau et al, 2020
昆虫纲 Insecta	灰蟋蟀 Gryllus veletis	滞育 Diapause	物种数↓、Shannon多样性指数↓ Observed species ↓, Shannon index ↓	厚壁菌门↓、变形菌门↑、拟杆菌门 Firmicutes ↓, Proteobacteria ↑, Bacteroidetes	-	Ferguson et al, 2018
弹尾纲 Collembola	Tomocerus cf jilinensis	活跃 Active	-	变形菌门、放线菌门、蓝菌门 Proteobacteria, Actinobacteria, Cyanobacteria	氨基酸代谢、碳水化合物代谢 Amino acid metabolism, Carbohydrate metabolism	Hao et al, 2020
腹足纲 Gastropoda	福寿螺 Pomacea canaliculata	半休眠 Semi-dormancy	Chao 1丰富度指数↓、 ACE丰富度指数↓、 Shannon多样性指数↓ Chao 1 index ↓, ACE index ↓, Shannon index ↓	变形菌门、厚壁菌门↑、梭杆菌门↑ Proteobacteria, Firmicutes ↑, Fusobacteria ↑	-	Li et al, 2022
双壳纲 Bivalvia	紫贻贝 Mytilus galloprovincialis	半休眠 Semi-dormancy	-	软壁菌门、假单胞菌门Mycoplasmatota, Pseudomonadota	-	Akter et al, 2023

宿主 Host		越冬策略 Overwintering strategy	越冬肠道细菌多样性 Gut bacterial diversity in winter	越冬肠道优势细菌门 Gut dominating bacterial phylum in winter	越冬肠道主要功能代谢 Gut main metabolic function in winter	参考文献 References
纲名 Class	种名 Species	越冬策略 Overwintering strategy	越冬肠道细菌多样性 Gut bacterial diversity in winter	越冬肠道优势细菌门 Gut dominating bacterial phylum in winter	越冬肠道主要功能代谢 Gut main metabolic function in winter	参考文献 References
哺乳纲 Mammalia	野牦牛 Bos mutus	活跃 Active	Chao 1丰富度指数↑ Chao 1 index ↑	拟杆菌门、厚壁菌门 Bacteroidetes, Firmicutes	脂肪细胞因子信号通路↑、脂肪酸降解↑ Adipocytokine signalling pathway ↑, fatty acid degradation ↑	Fu et al, 2021
哺乳纲 Mammalia	马铁菊头蝠 Rhinolophus ferrumequinum	冬眠 Hibernate	Chao 1丰富度指数↓、Shannon多样性指数↓ Chao 1 index ↓, Shannon index ↓	变形菌门、厚壁菌门↓ Proteobacteria, Firmicutes ↓	碳水化合物代谢↓、脂肪代谢↑ Carbohydrate metabolism ↓, lipid metabolism ↑	Xiao et al, 2019
鸟纲 Aves	艾草松鸡 Centrocercus urophasianus	活跃 Active	物种数↓、Shannon多样性指数↓ Observed species ↓, Shannon index ↓	欧陆森氏菌属↑, 巴斯德菌科↑ Olsenella ↑, Pasteurellaceae ↑	-	Drovetski et al, 2019
鸟纲 Aves	白额雁 Anser albifrons	活跃 Active	-	厚壁菌门、变形菌门、放线菌门 Firmicutes, Proteobacteria, Actinobacteri	碳水化合物代谢、氨基酸代谢 Carbohydrate metabolism, amino acid metabolism	Yang et al, 2016
两栖纲 Amphibia	东北林蛙 Rana dybowskii	冬眠 Hibernate	物种数↓、Chao 1丰富度指数↓、Shannon多样性指数↓ Observed species ↓, Chao 1 index ↓, Shannon index ↓	厚壁菌门↓、弯曲菌门↑ Firmicutes ↓, Campylobacterota ↑	-	Tong et al, 2023
两栖纲 Amphibia	扬子鳄 Alligator sinensis	冬眠 Hibernate	物种数↑、Chao 1丰富度指数↑、Shannon多样性指数 Observed species ↑, Chao 1 index ↑, Shannon index	变形菌门、拟杆菌门↑ Proteobacteria, Bacteroidetes ↑	粘蛋白寡糖降解酶↑ Mucin oligosaccharide- degrading enzymes ↑	Tang et al, 2019
昆虫纲 Insecta	西方蜜蜂 Apis mellifera	滞育 Diapause	Chao 1丰富度指数↓、Shannon多样性指数↓ Chao 1 index ↓, Shannon index ↓	根瘤菌科↑、肠杆菌科↓ Rhizobiaceae ↑, Enterobacteriaceae↓	-	Bleau et al, 2020
昆虫纲 Insecta	灰蟋蟀 Gryllus veletis	滞育 Diapause	物种数↓、Shannon多样性指数↓ Observed species ↓, Shannon index ↓	厚壁菌门↓、变形菌门↑、拟杆菌门 Firmicutes ↓, Proteobacteria ↑, Bacteroidetes	-	Ferguson et al, 2018
弹尾纲 Collembola	Tomocerus cf jilinensis	活跃 Active	-	变形菌门、放线菌门、蓝菌门 Proteobacteria, Actinobacteria, Cyanobacteria	氨基酸代谢、碳水化合物代谢 Amino acid metabolism, Carbohydrate metabolism	Hao et al, 2020
腹足纲 Gastropoda	福寿螺 Pomacea canaliculata	半休眠 Semi-dormancy	Chao 1丰富度指数↓、 ACE丰富度指数↓、 Shannon多样性指数↓ Chao 1 index ↓, ACE index ↓, Shannon index ↓	变形菌门、厚壁菌门↑、梭杆菌门↑ Proteobacteria, Firmicutes ↑, Fusobacteria ↑	-	Li et al, 2022
双壳纲 Bivalvia	紫贻贝 Mytilus galloprovincialis	半休眠 Semi-dormancy	-	软壁菌门、假单胞菌门Mycoplasmatota, Pseudomonadota	-	Akter et al, 2023

越冬动物肠道微生物多样性及功能研究进展

A review on gut microbial diversity and function of overwintering animals

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