Genome-wide analysis unveils the differentiated "external" and "internal" lectin system in the tropical sea cucumber Holothuria leucospilota.

To date, the understanding of lectin-related immunity in sea cucumbers remains limited. Through a comprehensive genome-wide analysis, 133 lectin genes were identified from Holothuria leucospilota, a sea cucumber species with high ecological and economic significance in the Pacific and Indian Oceans. These lectins were classified into five subtypes, with C-type lectin being the predominant form, and the presence of SUEL-like lectin and Malectin reported here for the first time in sea cucumbers. Transcriptomic analysis across twelve tissues and sixteen developmental stages revealed ubiquitous expression of H. leucospilota lectins. A key finding was the compartmentalization of lectin systems: SUEL-like lectins expressed in the body wall constitute an "external" defense system, while C-type lectins produced by coelomocytes form an "internal" immune system. This spatial and functional specialization reflects a sophisticated immune strategy in invertebrates, enabling targeted pathogen recognition at different bodily interfaces. Furthermore, distinct immune responses to Vibrio, LPS, and poly(I:C) were observed among different lectins. We also identified an ovary-specific C-type lectin, suggesting a potential role in early embryonic development. This study not only fills a knowledge gap regarding lectin genes in sea cucumbers but also establishes a broader framework for understanding complex immune mechanisms in echinoderms.