Comparative analysis of esophageal gland microbes between two body sizes of Gigantopelta aegis, a hydrothermal snail from the Southwest Indian Ridge.

Abstract

Microbial communities within animals provide nutritional foundation and energy supply for the hydrothermal ecosystem. The peltospirid snail Gigantopelta aegis forms large aggregation in the Longqi vent field on the Southwest Indian Ridge. This endemic species is characterized by a changeable diet and morphology, especially reflected in internal organs such as remarkably enlarged esophageal glands. Here, 16S full-length rRNA gene analysis was performed to compare the variations in esophageal gland microbiota between two body size groups (small and large) of G. aegis. Phyla Proteobacteria and Bacteroidetes were the dominant featured bacteria contributing to the microbial community. No significant differences between the small and large groups were revealed by the diversity index and principal component analysis (PCA) clustering. The differences were in the relative abundance of bacteria. Compared with small-sized snails, the larger ones housed more Thiogranum (9.94% to 34.86%) and fewer Sediminibacterium (29.38% to 4.54%). Functional prediction for all of the microbiota showed that the pathways related to metabolism appeared highly abundant in smaller G. aegis. However, for the larger ones, the most distinctive pathways were those of environmental information processing. Facultative symbiotic Sulfurovum was marked as a core node in the co-occurrence network and suggested an influence on habitat selection of G. aegis in hydrothermal fields. In summary, variations in bacteria composition and potential functions possibly reflected changes in the anatomical structure and dietary habits of G. aegis. These dominant bacteria shared capabilities in nutritional supplementation and ecological niche expansion in the host, potentially a key adaptation for hydrothermal survival.IMPORTANCEDominant in the Longqi hydrothermal vent Southwest Indian Ridge, Gigantopelta aegis was observed to undergo unique and significant morphological changes and diet shifts known as cryptometamorphosis. During this process, G. aegis developed a specialized bacteria-housing organ, the esophageal gland, in the later life stages. Our research discovered variations in esophageal gland microbes between different body size groups of snails. These bacteria were closely related to the development and health of G. aegis. Full-length 16S rRNA gene analysis revealed more Thiogranum and fewer Sediminibacterium, suggesting a potential association with environmental adaptation. In the small-sized group, the potential functions were enriched in metabolism, while in larger G. aegis individuals, predictions indicated adaptive functions such as environmental information processing. Also, symbiotic Sulfurovum could be one of the factors influencing the habitat selection of G. aegis. Understanding the complex relationship between benthic macrofauna and microbes helps us describe the mechanisms of survival in extreme environments.