The hydrolysis of sugar-containing compounds by glycoside hydrolases (GHs) plays essential roles in many major biological processes, but to date our systematic understanding of the functional diversity and evolution of GH families remains largely limited to a few well-studied terrestrial animals. Molluscs represent the largest marine phylum in the animal kingdom, and many of them are herbivorous that utilize algae as a main nutritional source, making them good subjects for studying the functional diversity and adaptive evolution of GH families. In the present study, we conducted genome-wide identification and functional and evolutionary analysis of all GH families across major molluscan lineages. We revealed that the remarkable expansion of the GH9, GH10, GH18 and GH20 families and the wide adoption of carbohydrate-binding modules in molluscan expanded GH families likely contribute to the efficient hydrolysis of marine algal polysaccharides and were involved in the consolidation of molluscan algae-feeding habits. Gene expression and network analysis revealed the hepatopancreas as the main organ for the prominent expression of approximately half of the GH families (well corresponding to the digestive roles of the hepatopancreas) and key or hub GHs in the coexpression gene network with potentially diverse functionalities. We also revealed the evolutionary signs of differential expansion and functional divergence of the GH family, which possibly contributed to lineage-specific adaptation. Systematic analysis of GH families at both genomic and transcriptomic levels provides important clues for understanding the functional divergence and evolution of GH gene families in molluscs in relation to their algae-feeding biology.

糖苷水解酶（GHs）对含糖化合物的水解在许多主要的生物学过程中起着至关重要的作用，但是迄今为止，我们对GH家族功能多样性和进化的系统理解仍然主要局限于一些经过充分研究的陆生动物。软体动物代表着动物界中最大的海洋动物门，其中许多是草食性的，它们利用藻类作为主要营养来源，使其成为研究GH家族功能多样性和适应性进化的良好对象。在本研究中，我们进行了主要软体动物谱系中所有GH家族的全基因组鉴定以及功能和进化分析。我们发现GH9，GH10，GH18和GH20家族以及在软体动物扩展的GH系列中碳水化合物结合模块的广泛采用可能有助于海洋藻类多糖的有效水解，并参与巩固软体动物藻类的摄食习性。基因表达和网络分析表明，肝胰腺是主要表达器官，约占一半的GH家族（与肝胰腺的消化作用相对应）的突出表达，并且在共同表达基因网络中关键或中枢GH具有潜在的多样性功能。我们还揭示了GH家族差异扩展和功能差异的进化迹象，这可能有助于谱系特异性适应。