“ <i>Candidatus</i> Desulfobulbus rimicarensis,” an Uncultivated Deltaproteobacterial Epibiont from the Deep-Sea Hydrothermal Vent Shrimp <i>Rimicaris exoculata</i>

Abstract

The deep-sea hydrothermal vent shrimp <i>Rimicaris exoculata</i> largely depends on a dense epibiotic chemoautotrophic bacterial community within its enlarged cephalothoracic chamber. However, our understanding of shrimp-bacterium interactions is limited. In this report, we focused on the deltaproteobacterial epibiont of <i>R. exoculata</i> from the relatively unexplored South Mid-Atlantic Ridge. A nearly complete genome of a <i>Deltaproteobacteria</i> epibiont was binned from the assembled metagenome. Whole-genome phylogenetic analysis reveals that it is affiliated with the genus <i>Desulfobulbus</i>, representing a potential novel species for which the name "<i>Candidatus</i> Desulfobulbus rimicarensis" is proposed. Genomic and transcriptomic analyses reveal that this bacterium utilizes the Wood-Ljungdahl pathway for carbon assimilation and harvests energy via sulfur disproportionation, which is significantly different from other shrimp epibionts. Additionally, this epibiont has putative nitrogen fixation activity, but it is extremely active in directly taking up ammonia and urea from the host or vent environments. Moreover, the epibiont could be distinguished from its free-living relatives by various features, such as the lack of chemotaxis and motility traits, a dramatic reduction in biosynthesis genes for capsular and extracellular polysaccharides, enrichment of genes required for carbon fixation and sulfur metabolism, and resistance to environmental toxins. Our study highlights the unique role and symbiotic adaptation of <i>Deltaproteobacteria</i> in deep-sea hydrothermal vent shrimps.<b>IMPORTANCE</b> The shrimp <i>Rimicaris exoculata</i> represents the dominant faunal biomass at many deep-sea hydrothermal vent ecosystems along the Mid-Atlantic Ridge. This organism harbors dense bacterial epibiont communities in its enlarged cephalothoracic chamber that play an important nutritional role. <i>Deltaproteobacteria</i> are ubiquitous in epibiotic communities of <i>R. exoculata</i>, and their functional roles as epibionts are based solely on the presence of functional genes. Here, we describe "<i>Candidatus</i> Desulfobulbus rimicarensis," an uncultivated deltaproteobacterial epibiont. Compared to campylobacterial and gammaproteobacterial epibionts of <i>R. exoculata</i>, this bacterium possessed unique metabolic pathways, such as the Wood-Ljungdahl pathway, as well as sulfur disproportionation and nitrogen fixation pathways. Furthermore, this epibiont can be distinguished from closely related free-living <i>Desulfobulbus</i> strains by its reduced genetic content and potential loss of functions, suggesting unique adaptations to the shrimp host. This study is a genomic and transcriptomic analysis of a deltaproteobacterial epibiont and largely expands the understanding of its metabolism and adaptation to the <i>R. exoculata</i> host.