Simon F. S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China.
School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales, Australia.
Mol Ecol. 2024 Jun;33(12):e17377. doi: 10.1111/mec.17377. Epub 2024 May 7.
The acquisition of microbial symbionts enables animals to rapidly adapt to and exploit novel ecological niches, thus significantly enhancing the evolutionary fitness and success of their hosts. However, the dynamics of host-microbe interactions and their evolutionary implications remain largely underexplored in marine invertebrates. Crabs of the family Sesarmidae (Crustacea: Brachyura) are dominant inhabitants of mangrove forests and are considered keystone species there. Their rapid diversification, particularly after adopting a plant-feeding lifestyle, is believed to have been facilitated by symbiotic gut microbes, enabling successful colonization of intertidal and terrestrial environments. To investigate the patterns and mechanisms shaping the microbial communities and the role of microbes in the evolution of Sesarmidae, we characterized and compared the gut microbiome compositions across 43 crab species from Sesarmidae and other mangrove-associated families using 16S metabarcoding. We found that the gut microbiome assemblages in crabs are primarily determined by host identity, with a secondary influence from environmental factors such as microhabitat and sampling location, and to a lesser extent influenced by biological factors such as sex and gut region. While patterns of phylosymbiosis (i.e. when microbial community relationships recapitulate the phylogeny of their hosts) were consistently observed in all beta-diversity metrics analysed, the strength of phylosymbiosis varied across crab families. This suggests that the bacterial assemblages in each family were differentially shaped by different degrees of host filtering and/or other evolutionary processes. Notably, Sesarmidae displayed signals of cophylogeny with its core gut bacterial genera, which likely play crucial functional roles in their hosts by providing lignocellulolytic enzymes, essential amino acids, and fatty acids supplementation. Our results support the hypothesis of microbial contribution to herbivory and terrestrialization in mangrove crabs, highlighting the tight association and codiversification of the crab holobiont.
动物通过获得微生物共生体能够快速适应和开拓新的生态位，从而显著提高宿主的进化适应性和成功度。然而，宿主-微生物相互作用的动态及其进化意义在海洋无脊椎动物中仍很大程度上未被探索。扇蟹科（甲壳纲：短尾下目）的螃蟹是红树林的主要居民，被认为是那里的关键物种。它们的快速多样化，特别是在采用植物食性的生活方式之后，据信是由共生肠道微生物促成的，这使得它们能够成功地在潮间带和陆地环境中殖民。为了研究塑造微生物群落的模式和机制以及微生物在扇蟹科进化中的作用，我们使用 16S 代谢组学对来自扇蟹科和其他与红树林相关的科的 43 种螃蟹的肠道微生物组组成进行了特征描述和比较。我们发现，螃蟹的肠道微生物群落主要由宿主身份决定，其次是微生境和采样地点等环境因素，以及性别和肠道区域等生物学因素的次要影响。虽然在所有分析的β多样性指标中都一致观察到了微生物共生关系的模式（即当微生物群落关系概括其宿主的系统发育时），但在不同的蟹科中，微生物共生关系的强度存在差异。这表明，每个科的细菌组合是由宿主过滤和/或其他进化过程的不同程度差异塑造的。值得注意的是，扇蟹科与其核心肠道细菌属显示出共进化信号，这些细菌属可能通过提供木质纤维素酶、必需氨基酸和脂肪酸补充来在其宿主中发挥关键功能作用。我们的研究结果支持微生物对红树林螃蟹草食性和陆地化的贡献假说，强调了螃蟹整体共生体的紧密联系和共同进化。
