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. 2017 Mar 15;12(3):e0172543.
doi: 10.1371/journal.pone.0172543. eCollection 2017.

Investigation of Bacterial Communities Within the Digestive Organs of the Hydrothermal Vent Shrimp Rimicaris Exoculata Provide Insights Into Holobiont Geographic Clustering

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Investigation of Bacterial Communities Within the Digestive Organs of the Hydrothermal Vent Shrimp Rimicaris Exoculata Provide Insights Into Holobiont Geographic Clustering

Dominique A Cowart et al. PLoS One. .
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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.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Geographic locations of three hydrothermal vents along the Mid-Atlantic Ridge (MAR).
Hydrothermal vent locations from where Rimicaris exoculata were sampled for this study.
Fig 2
Fig 2. Multidimensional scaling (MDS) analyses for Rimicaris exoculata bacterial communities.
(A) Clustering pattern by vents, with colored circles representing the vent location from where each sample was collected. (B) Clustering pattern by vent, with colored shapes and letters denoting the specific categories for each sample. Each MDS was implemented using Bray-Curtis similarity matrices, calculated in PAST [34]. The 95% concentration ellipses estimate a region where 95% of the population points are expected to fall. “Orange” indicates juveniles, whose carapace is an orange color.
Fig 3
Fig 3. Frequencies of identified bacterial classes across the three life stages at Logatchev.
Four main classes are identified across Rimicaris exoculata life stages. “Other classes” contain nine or more less common groups.
Fig 4
Fig 4. Geographic networks for operational taxonomic units (OTUs) assigned to bacterial classes Deferribacteres and Mollicutes.
(A) OTU “denovo 10553”, assigned to Deferribacteres, was composed of 504 sequences. (B) OTU “denovo 6152”, assigned to Mollicutes, was composed of 691 sequences. Networks were drawn with median-joining calculation to illustrate the clustering of haplotypes; links are not proportional to the number of mutations and therefore, do not illustrate evolutionary divergence between the nodes.
Fig 5
Fig 5. Geographic network for an operational taxonomic unit (OTU) assigned to bacterial class Epsilonproteobacteria (denovo 10123).
OTU “denovo 10123” was composed of 668 sequences. Network was drawn with median-joining calculation to illustrate the clustering of haplotypes; links are not proportional to the number of mutations and therefore, do not illustrate evolutionary divergence between the nodes.

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Grant support

This work was supported the by Hermione project (FP7, European Union) to MACB and SAH; DAC and LD were supported by post-doctoral contracts at Ifremer.
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