Gill chamber and gut microbial communities of the hydrothermal shrimp Rimicaris chacei Williams and Rona 1986: A possible symbiosis.

Vincent Apremont,Valérie Cueff-Gauchard,Magali Zbinden,Laure Corbari,Marie-Anne Cambon-Bonavita,Florence Pradillon,David François,Chih-Horng Kuo

doi:10.1371/journal.pone.0206084

Abstract

Rimicaris chacei Williams and Rona 1986, formerly named as Chorocaris chacei, is a caridean shrimp living in deep-sea hydrothermal ecosystems. This shrimp is endemic to the Mid Atlantic Ridge (MAR) and lives at the periphery of aggregates of its well-known congeneric R. exoculata Williams and Rona 1986. Contrasting with the very dense and mobile clusters formed by R. exoculata, R. chacei lives in small groups of several individuals that are not very mobile. Although devoid of the characteristic hypertrophied cephalothorax of R. exoculata, which harbors the ectosymbionts, a microbial community has also been reported in the cephalothorax of R. chacei. Previous data on morphology, behavior and isotopic values indicate a diet based on a combination of feeding on its epibiotic bacteria and scavenging or occasional predation. In this study, our objective was to describe, for the first time, the distribution, morphology and phylogeny of the microbial communities associated with R. chacei. This species is significantly less studied than R. exoculata, but nevertheless represents the only other known example of symbiosis in crustaceans of MAR hydrothermal vent sites. Microbial communities have been observed at the same locations as in R. exoculata (mouthparts, branchiostegites and digestive tract). However, in R. chacei, the surfaces occupied by the bacteria are smaller. The main lineages are affiliated to Epsilon and Gammaproteobacteria in the cephalothorax and to Deferribacteres, Mollicutes, Epsilon and Gammaproteobacteria in the digestive tract. Comparison with the well-described bacterial communities of R. exoculata and hypotheses about the role of these communities in R. chacei are discussed.

Highlights

We provide a detailed description and characterization of the association between R. chacei and its microbial communities and we draw hypotheses about their roles in comparison with those found in R. exoculata symbiosis
The coccobacillus morphotype (Fig 3E) presented stacks of internal membranes characteristic of methanotrophic-like bacteria type I (Fig 3D) [39]. These occurred in small aggregates of four to seven bacteria. All these morphotypes were present on the branchiostegites and scaphognathites of the shrimp from each studied vent site, except for large filamentous morphotypes, which were not observed on TAG specimen, and methanotrophic-like bacteria, which were not observed on TAG or Snake Pit specimens
The bacteriophore tissues are less developed in R. chacei than in R. exoculata, the cephalothoracic community of R. chacei forms a dense mat on the anterior third of the inner side of the branchiostegites and on both sides of the scaphognathites (Fig 1A and 1B, [12])