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

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

doi:10.1371/journal.pone.0172543

Cited by 14 publications

(27 citation statements)

References 55 publications

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“…Phylogenetic analyses on R . exoculata gut symbionts have led to the identification of four major clades: Mollicutes, Deferribacteres, Gammaproteobacteria and Epsilonproteobacteria [ 6 – 8 , 57 ]. The same four phylotypes are well represented in our R .…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2018

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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.

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Section: Discussionmentioning

confidence: 99%

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

et al. 2018

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“…Nonetheless, here we find that it is the sole order that significantly increased in relative abundance with increasing oil exposure levels. Deferribacterales has a wide environmental distribution and members have been found in hydrothermal vent communities [ 57 ], the gut microbiota of the hydrothermal shrimp Rimicaris exoculate [ 58 ] and in rodents [ 59 ]. Yet interestingly this order has also been found in high abundance in subsea petroleum reservoirs [ 60 ].…”

Section: Discussionmentioning

confidence: 99%

Gastrointestinal microbial community changes in Atlantic cod (Gadus morhua) exposed to crude oil

et al. 2018

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BackgroundThe expansion of offshore oil exploration increases the risk of marine species being exposed to oil pollution in currently pristine areas. The adverse effects of oil exposure through toxic properties of polycyclic aromatic hydrocarbons (PAHs) have been well studied in Atlantic cod (Gadus morhua). Nevertheless, the fate of conjugated metabolites in the intestinal tract and their effect on the diversity of intestinal microbial community in fish is less understood. Here, we investigated the intestinal microbial community composition of Atlantic cod after 28 days of exposure to crude oil (concentration range 0.0–0.1 mg/L).ResultsAnalysis of PAH metabolites in bile samples confirmed that uptake and biotransformation of oil compounds occurred as a result of the exposure. Various evidence for altered microbial communities was found in fish exposed to high (0.1 mg/L) and medium (0.05 mg/L) concentrations of oil when compared to fish exposed to low oil concentration (0.01 mg/L) or no oil (control). First, altered banding patterns were observed on denaturing gradient gel electrophoresis for samples pooled from each treatment group. Secondly, based on 16S rRNA sequences, higher levels of oil exposure were associated with a loss of overall diversity of the gut microbial communities. Furthermore, 8 operational taxonomic units (OTUs) were found to have significantly different relative abundances in samples from fishes exposed to high and medium oil concentrations when compared to samples from the control group and low oil concentration. Among these, only one OTU, a Deferribacterales, had increased relative abundance in samples from fish exposed to high oil concentration.ConclusionsThe results presented herein contribute to a better understanding of the effects of oil contamination on the gut microbial community changes in fish and highlight the importance of further studies into the area. Our findings suggest that increased relative abundance of bacteria belonging to the order Deferribacterales may be indicative of exposure to oil at concentrations higher than 0.05 mg/L.Electronic supplementary materialThe online version of this article (10.1186/s12866-018-1171-2) contains supplementary material, which is available to authorized users.

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“…The bacterial diversity in the midgut is largely represented by 3 major groups: Deferribacteres, Mollicutes and Campylobacteria. Gammaproteobacteria are also present to a lesser extent (Zbinden & Cambon-Bonavita 2003, Durand et al 2010, Cowart et al 2017. This diversity is relatively restricted compared to the environmental one (Durand et al 2015).…”

Section: Bacterial Phylogenetic Diversitymentioning

confidence: 99%

“…Intact rods and cocci were observed within the gut content (Zbinden & Cambon-Bonavita 2003). Some of them are probably transient, but some may be part of a specific resident microflora (Zbinden & Cambon-Bonavita 2003, Durand et al 2010, Cowart et al 2017.…”

Section: Bacterial Localization and Morphological Diversitymentioning

confidence: 99%

Rimicaris exoculata: biology and ecology of a shrimp from deep-sea hydrothermal vents associated with ectosymbiotic bacteria

Zbinden

Cambon-Bonavita

2020

Mar. Ecol. Prog. Ser.

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Rimicaris exoculata, the ‘blind shrimp,’ is the most abundant species living on active hydrothermal edifices at deep-sea vents of the Mid-Atlantic Ridge. Its unusually enlarged branchial chamber houses a dense ectosymbiotic community of chemoautotrophic bacteria. Long debated, shrimp nutrition has been proven to be a kind of osmotrophy, whereby small organic molecules produced by the symbionts pass through the integument of the shrimp directly into the circulatory system, rather than through the digestive system. The broad phylogenetic and metabolic diversity of this epibiotic community suggests a highly flexible and adjustable microbial consortium, adapted to the chemically contrasting environments inhabited by the shrimp. To cope with the highly fluctuating oxygen and temperature conditions of its habitat, R. exoculata possesses hemocyanin with a strong oxygen affinity, and has developed both molecular and behavioral responses to heat stresses. If R. exoculata is able to detect very dim light or chemical compounds emitted by vents, the relatively small visual and olfactory areas in the brain, along with the disproportionately enlarged higher centers, argue for a significant involvement of navigational skills using learning and place memory to orient itself within its aphotic environment. This shrimp undergoes unconventional larval development, with a primary lecithotrophic stage followed by an extended planktotrophic period, allowing a huge potential for dispersion. In light of mining licenses posing a threat for deep-sea environments, this species is a model still to be studied to better understand life in extreme deep-sea ecosystems at the global scale of an ocean.

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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

Cited by 14 publications

References 55 publications

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

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

Gastrointestinal microbial community changes in Atlantic cod (Gadus morhua) exposed to crude oil

Rimicaris exoculata: biology and ecology of a shrimp from deep-sea hydrothermal vents associated with ectosymbiotic bacteria

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