Investigation of bacterial communities within the digestive organs of the hydrothermal vent shrimp Rimicaris exoculata provide insights into holobiont geographic clustering.

Dominique A Cowart,Lucile Durand,Marie-Anne Cambon-Bonavita,Sophie Arnaud-Haond

doi:10.1371/journal.pone.0172543

Abstract

Prokaryotic communities forming symbiotic relationships with the vent shrimp, Rimicaris exoculata, are well studied components of hydrothermal ecosystems at the Mid-Atlantic Ridge (MAR). Despite the tight link between host and symbiont, the observed lack of spatial genetic structure seen in R. exoculata contrasts with the geographic differentiation detected in specific bacterial ectosymbionts. The geographic clustering of bacterial lineages within a seemingly panmictic host suggests either the presence of finer scale restriction to gene flow not yet detected in the host, horizontal transmission (environmental selection) of its endosymbionts as a consequence of unique vent geochemistry, or vertically transmitted endosymbionts that exhibit genetic differentiation. To identify which hypothesis best fits, we tested whether bacterial assemblages exhibit differentiation across sites or host populations by performing a 16S rRNA metabarcoding survey on R. exoculata digestive prokaryote samples (n = 31) taken from three geochemically distinct vents across MAR: Rainbow, Trans-Atlantic Geotraverse (TAG) and Logatchev. Analysis of communities across two organs (digestive tract, stomach), three molt colors (white, red, black) and three life stages (eggs, juveniles, adults) also provided insights into symbiont transmission mode. Examining both whole communities and operational taxonomic units (OTUs) confirmed the presence of three main epibionts: Epsilonproteobacteria, Mollicutes and Deferribacteres. With these findings, we identified a clear pattern of geographic segregation by vent in OTUs assigned to Epsilonproteobacteria. Additionally, we detected evidence for differentiation among all communities associated to vents and life stages. Overall, results suggest a combination of environmental selection and vertical inheritance of some of the symbiotic lineages.

Highlights

Deep-sea hydrothermal vent ecosystems are characterized by low oxygen, temperature extremes and toxic compounds, during an eruption event [1]
Our pyrosequencing of the bacterial communities associated to the vent shrimp Rimicaris exoculata produced a total of 366,134 raw sequence reads
The sequence dataset was clustered into 1,726 representative operational taxonomic units (OTUs); 1,621 (94%) of these OTUs were taxonomically assigned to homologs in the RDP database

Summary

Introduction

Deep-sea hydrothermal vent ecosystems are characterized by low oxygen, temperature extremes and toxic compounds, during an eruption event [1]. Bacterial communities serve as the primary producers at these ecosystems and often form symbiotic relationships with invertebrate fauna, including the alvinocarid shrimp, Rimicaris exoculata [4]. One community is located in the inner surfaces of its gill chamber and mainly composed of Epsilon, Gamma, Zeta and Deltaproteobacteria, known as sulfide, iron or methane oxidizers that obtain nutrition from the vent activity [8,9,10,11,12,13,14,15,16]. Most of the gill chamber symbionts appear to be locally acquired, likely being obtained from the surrounding seawater [18, 19]. Previous biogeographic analyses tend towards a local distribution of the symbionts, suggesting possible horizontal transmission [14]

Methods

Results

Discussion

Conclusion