Metagenomic and metatranscriptomic analyses reveal minor-yet-crucial roles of gut microbiome in deep-sea hydrothermal vent snail

Abstract

Abstract Background Marine animals often exhibit complex symbiotic relationship with gut microbes to attain better use of the available resources. Many animals endemic to deep-sea chemosynthetic ecosystems host chemoautotrophic bacteria endocellularly, and they are thought to rely entirely on these symbionts for energy and nutrition. Numerous investigations have been conducted on the interdependence between these animal hosts and their chemoautotrophic symbionts. The provannid snail Alviniconcha marisindica from the Indian Ocean hydrothermal vent fields hosts a Campylobacterial endosymbiont in its gill. Unlike many other chemosymbiotic animals, the gut of A. marisindica is reduced but remains functional; yet the contribution of gut microbiomes and their interactions with the host remain poorly characterised. Results Metagenomic and metatranscriptomic analyses showed that the gut microbiome of A. marisindica plays key nutritional and metabolic roles. The composition and relative abundance of gut microbiota of A. marisindica were different from those of snails that do not depend on endosymbiosis. The relative abundance of microbial taxa was similar amongst three individuals of A. marisindica with significant inter-taxa correlations. These correlations suggest the potential for interactions between taxa that may influence community assembly and stability. Functional profiles of the gut microbiome revealed thousands of additional genes that assist in the use of vent-supplied inorganic compounds (autotrophic energy source), digest host-ingested organics (carbon source), and recycle the metabolic waste of the host. In addition, members of five taxonomic classes have the potential to form slime capsules to protect themselves from the host immune system, thereby contributing to homeostasis. Gut microbial ecology and its interplay with the host thus contribute to the nutritional and metabolic demands of A. marisindica. Conclusions The findings advance the understanding of how deep-sea chemosymbiotic animals use available resources through contributions from gut microbiota. Gut microbiota may be critical in the survival of invertebrate hosts with autotrophic endosymbionts in extreme environments.