Metagenomic analysis reveals hidden links between gut microbes and habitat adaptation among cave and surface dwelling Sinocyclocheilus species

Intestinal microbes are closely related to vital functions for the host such as food digestion and nutrient absorption, which plays an important role in enhancing host adaptability. As a natural “laboratory,” a cave habitat provides an outstanding model for understanding the significance of gut microbes and feeding habits in a host’s habitat adaptability. However, research on the relationship between gut microbes, feeding habits, and the adaptability of troglobites is insufficient. In this study, we compared the characteristics of the intestinal microbes of Sinocyclocheilus cavefishes and surface fishes and further established the relationship between intestinal and habitat microbes. Furthermore, we also conducted eDNA (metabarcoding) analysis on environmental samples to clarify the composition of potential food resources in habitats of the Sinocyclocheilus cave and surface fishes. The results show that the structure of Sinocyclocheilus gut microbes is more related to the ecological type (habitat type) than phylogenetic relationships. However, the horizontal transfer of habitat microbes is one source of fish gut microbes, but the host shows a strong selection for inherent microbes as predominant microorganisms. The difference in composition and structure of gut microbes, especially predominant microbes, can enhance the adaptability of the two Sinocyclocheilus fish types from the perspectives of food intake, nutrient utilization, and harmful substance metabolism. Such links eventually form a closed loop of habitat adaptability through food resources, predation pattern, intestinal flora, digestive and absorptive capacity, and feeding habits and preferences. The obtained results facilitate our understanding of the significance of fish gut microbes to habitat adaptation and provide a new perspective for studying the adaptive mechanisms of cave fishes.

肠道微生物与宿主的食物消化、营养吸收等核心生命功能密切相关，对提升宿主适应性具有关键作用。洞穴生境作为天然的“实验室”，为探究肠道微生物与摄食习性在宿主生境适应性中的意义提供了理想模型。然而，当前针对肠道微生物、摄食习性与洞栖动物适应性之间关联的研究仍较为不足。本研究对比了金线鲃属（Sinocyclocheilus）洞穴鱼类与地表鱼类的肠道微生物特征，并进一步构建了肠道微生物与生境微生物之间的关联网络。此外，我们还对环境样本开展了eDNA（代谢条形码测序，metabarcoding）分析，以明确金线鲃属洞穴鱼类与地表鱼类栖息环境中潜在食物资源的组成。研究结果表明，金线鲃肠道微生物的群落结构与其生态型（生境类型）的相关性显著高于其系统发育关系。尽管生境微生物的水平转移是鱼类肠道微生物的来源之一，但宿主对固有微生物具有强烈的筛选作用，使其成为肠道内的优势菌群。肠道微生物群落组成与结构的差异，尤其是优势菌群的差异，可从食物摄入、营养利用及有害物质代谢等多个维度提升两类金线鲃的适应性。这种关联最终通过食物资源、捕食模式、肠道菌群、消化吸收能力以及摄食习性与偏好，形成了一条闭合的生境适应性循环通路。本研究所得结果有助于深入理解鱼类肠道微生物对生境适应的重要意义，并为探究洞穴鱼类的适应性机制提供了全新的研究视角。