Specificity of benthic invertebrate gill-associated microbiome contributes to host fitness to localized heterogeneous environment in the cold seep.

The deep hydrocarbon fluids discharged into the water column at cold seeps create diverse and heterogeneous habitats on the seafloor. Symbiosis is essential for the survival of marine life in extreme deep-sea environments. Although the symbiotic relationship between chemoautotrophic bacteria and invertebrates has been reported, our understanding of these host-microbe interactions under heterogeneous environment remains limited. In this study, we evaluated the bacterial community structures, histological and subcellular localization, and potential functions of the gill microbiomes of six invertebrates in the Haima cold seep, South China Sea. The results showed distinct gill-associated microbiomes in these six invertebrates. Gigantidas haimaensis and Archivesica marissinica exhibit a highly dependent symbiotic relationship with their intracellular gill symbionts, characterized by a simple composition. In contrast, Alvinocaris longirostris, Shinkaia crosnieri, Phymorhynchus buccinoides, and Paraescarpia echinospica display a loosely dependent association with their extracellular gill-associated microbes, which are notably complex in composition. Moreover, gill microbiome specificity was seen among six invertebrates and host selection could be an underlying mechanism. The potential functional components of these six invertebrate gill microbiomes contribute to host fitness in heterogeneous local environments. The results obtained from our study provide insights into the ecology and evolution of host-microbe interactions and the underlying mechanisms in extreme marine environments. This information is critical for predicting the responses of benthic fauna to environmental changes in cold seeps.