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

Type Article
Date 2017-03
Language English
Author(s) Cowart DominiqueORCID1, 5, Durand Lucile2, Cambon-Bonavita Marie-AnneORCID2, 3, 4, Arnaud-Haond SophieORCID1
Affiliation(s) 1 : IFREMER, UMR MARBEC Marine Biodivers Exploitat & Conservat, BP 17, Sete, France.
2 : IFREMER, Lab Microbiol Environm Extremes, Dept Ressources Phys & Ecosyst Fond Mer REM, UMR6197,ZI Pointe Diable,CS 10070, Plouzane, France.
3 : IFREMER, UBO, CNRS, UMR 6197, IUEM Rue Dumont dUrville, Plouzane, France.
4 : IFREMER, CNRS, UMR 6197, UBO, IUEM Rue Dumont dUrville, Plouzane, France.
5 : Univ Illinois, Dept Anim Biol, Urbana, IL USA.
Source Plos One (1932-6203) (Public Library Science), 2017-03 , Vol. 12 , N. 3 , P. e0172543 (1-22)
DOI 10.1371/journal.pone.0172543
WOS© Times Cited 3
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.
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Publisher's official version 22 1 MB Open access
S1 Fig. 16S Maximum Likelihood (ML) consensus boostrap tree for Epsilonproteobacteria. 1 198 KB Open access
S2 Fig. 16S Maximum Likelihood (ML) consensus boostrap tree for Gammaproteobacteria. 1 200 KB Open access
S3 Fig. 16S Maximum Likelihood (ML) consensus boostrap tree for Mollicutes. 1 161 KB Open access
S4 Fig. 16S Maximum Likelihood (ML) consensus boostrap tree for Deferribacteres. 1 197 KB Open access
S5 Fig. Multidimensional Scaling (MDS) analyses for Rimicaris exoculata bacterial communities, including unidentified bacteria. 1 305 KB Open access
S6 Fig. Frequencies of identified bacterial classes for the three life stages at Logatchev, including unidentified bacteria. 1 152 KB Open access
S7 Fig. Species count and species richness for molt colors at Rainbow (A) and life stages at Logatchev (B). 1 171 KB Open access
S8 Fig. Geographic network for Operational Taxonomic Unit (OTU) assigned to Gammaproteobacteria. 1 148 KB Open access
S1 File. QIIME workflows and commands. 1 167 KB Open access
S2 File. ANOVA testing of OTU frequency among groups, performed using the group_significance.py script in QIIME [29]. 519 KB Open access
S1 Table. Geographic coordinates, depth, year(s) and number of samples sequenced for Rimicaris exoculata collections from three vents along the Mid-Atlantic Ridge (MAR) 1 77 KB Open access
S2 Table. Rimicaris exoculata sample counts by organs, molts and life stage categories. 1 75 KB Open access
S3 Table. Metadata for each sample. 1 111 KB Open access
S4 Table. Strategy for statistically testing the rejection of the null hypothesis of homogeneity of bacterial communities across molt stages, organs, life stages and vents. 1 80 KB Open access
S5 Table. Counts and percentages of OTUs that were described only to domain level ‘bacteria’ for each sample (unclassified bacteria). 1 142 KB Open access
S6 Table. ANOSIM test results for dataset including unclassified bacteria. 1 87 KB Open access
S7 Table. Alpha diversity indices, species count and species richness (Chao1 and standard error) for dataset including unclassified bacteria. 1 86 KB Open access
S8 Table. Frequency of OTUs assigned to class for each vent, including unclassified bacteria. 1 94 KB Open access
S9 Table. ANOSIM and PERMANOVA results excluding unclassified bacteria. 1 105 KB Open access
S10 Table. Frequency of OTUs assigned to class for each vent, excluding unclassified bacteria. 1 91 KB Open access
S11 Table. Qualitative results of the most common haplotypes. 2 116 KB Open access
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Cowart Dominique, Durand Lucile, Cambon-Bonavita Marie-Anne, Arnaud-Haond Sophie (2017). Investigation of bacterial communities within the digestive organs of the hydrothermal vent shrimp Rimicaris exoculata provide insights into holobiont geographic clustering. Plos One, 12(3), e0172543 (1-22). Publisher's official version : https://doi.org/10.1371/journal.pone.0172543 , Open Access version : https://archimer.ifremer.fr/doc/00376/48705/