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Metatranscriptional Response of Chemoautotrophic Ifremeria nautilei Endosymbionts to Differing Sulfur Regimes

Endosymbioses between animals and chemoautotrophic bacteria are ubiquitous at hydrothermal vents. These environments are distinguished by high physico-chemical variability, yet we know little about how these symbioses respond to environmental fluctuations. We therefore examined how the γ-proteobacte...

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Autores principales: Seston, Sherry L., Beinart, Roxanne A., Sarode, Neha, Shockey, Abigail C., Ranjan, Piyush, Ganesh, Sangita, Girguis, Peter R., Stewart, Frank J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4949241/
https://www.ncbi.nlm.nih.gov/pubmed/27486438
http://dx.doi.org/10.3389/fmicb.2016.01074
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author Seston, Sherry L.
Beinart, Roxanne A.
Sarode, Neha
Shockey, Abigail C.
Ranjan, Piyush
Ganesh, Sangita
Girguis, Peter R.
Stewart, Frank J.
author_facet Seston, Sherry L.
Beinart, Roxanne A.
Sarode, Neha
Shockey, Abigail C.
Ranjan, Piyush
Ganesh, Sangita
Girguis, Peter R.
Stewart, Frank J.
author_sort Seston, Sherry L.
collection PubMed
description Endosymbioses between animals and chemoautotrophic bacteria are ubiquitous at hydrothermal vents. These environments are distinguished by high physico-chemical variability, yet we know little about how these symbioses respond to environmental fluctuations. We therefore examined how the γ-proteobacterial symbionts of the vent snail Ifremeria nautilei respond to changes in sulfur geochemistry. Via shipboard high-pressure incubations, we subjected snails to 105 μM hydrogen sulfide (LS), 350 μM hydrogen sulfide (HS), 300 μM thiosulfate (TS) and seawater without any added inorganic electron donor (ND). While transcript levels of sulfur oxidation genes were largely consistent across treatments, HS and TS treatments stimulated genes for denitrification, nitrogen assimilation, and CO(2) fixation, coincident with previously reported enhanced rates of inorganic carbon incorporation and sulfur oxidation in these treatments. Transcripts for genes mediating oxidative damage were enriched in the ND and LS treatments, potentially due to a reduction in O(2) scavenging when electron donors were scarce. Oxidative TCA cycle gene transcripts were also more abundant in ND and LS treatments, suggesting that I. nautilei symbionts may be mixotrophic when inorganic electron donors are limiting. These data reveal the extent to which I. nautilei symbionts respond to changes in sulfur concentration and species, and, interpreted alongside coupled biochemical metabolic rates, identify gene targets whose expression patterns may be predictive of holobiont physiology in environmental samples.
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spelling pubmed-49492412016-08-02 Metatranscriptional Response of Chemoautotrophic Ifremeria nautilei Endosymbionts to Differing Sulfur Regimes Seston, Sherry L. Beinart, Roxanne A. Sarode, Neha Shockey, Abigail C. Ranjan, Piyush Ganesh, Sangita Girguis, Peter R. Stewart, Frank J. Front Microbiol Microbiology Endosymbioses between animals and chemoautotrophic bacteria are ubiquitous at hydrothermal vents. These environments are distinguished by high physico-chemical variability, yet we know little about how these symbioses respond to environmental fluctuations. We therefore examined how the γ-proteobacterial symbionts of the vent snail Ifremeria nautilei respond to changes in sulfur geochemistry. Via shipboard high-pressure incubations, we subjected snails to 105 μM hydrogen sulfide (LS), 350 μM hydrogen sulfide (HS), 300 μM thiosulfate (TS) and seawater without any added inorganic electron donor (ND). While transcript levels of sulfur oxidation genes were largely consistent across treatments, HS and TS treatments stimulated genes for denitrification, nitrogen assimilation, and CO(2) fixation, coincident with previously reported enhanced rates of inorganic carbon incorporation and sulfur oxidation in these treatments. Transcripts for genes mediating oxidative damage were enriched in the ND and LS treatments, potentially due to a reduction in O(2) scavenging when electron donors were scarce. Oxidative TCA cycle gene transcripts were also more abundant in ND and LS treatments, suggesting that I. nautilei symbionts may be mixotrophic when inorganic electron donors are limiting. These data reveal the extent to which I. nautilei symbionts respond to changes in sulfur concentration and species, and, interpreted alongside coupled biochemical metabolic rates, identify gene targets whose expression patterns may be predictive of holobiont physiology in environmental samples. Frontiers Media S.A. 2016-07-19 /pmc/articles/PMC4949241/ /pubmed/27486438 http://dx.doi.org/10.3389/fmicb.2016.01074 Text en Copyright © 2016 Seston, Beinart, Sarode, Shockey, Ranjan, Ganesh, Girguis and Stewart. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Seston, Sherry L.
Beinart, Roxanne A.
Sarode, Neha
Shockey, Abigail C.
Ranjan, Piyush
Ganesh, Sangita
Girguis, Peter R.
Stewart, Frank J.
Metatranscriptional Response of Chemoautotrophic Ifremeria nautilei Endosymbionts to Differing Sulfur Regimes
title Metatranscriptional Response of Chemoautotrophic Ifremeria nautilei Endosymbionts to Differing Sulfur Regimes
title_full Metatranscriptional Response of Chemoautotrophic Ifremeria nautilei Endosymbionts to Differing Sulfur Regimes
title_fullStr Metatranscriptional Response of Chemoautotrophic Ifremeria nautilei Endosymbionts to Differing Sulfur Regimes
title_full_unstemmed Metatranscriptional Response of Chemoautotrophic Ifremeria nautilei Endosymbionts to Differing Sulfur Regimes
title_short Metatranscriptional Response of Chemoautotrophic Ifremeria nautilei Endosymbionts to Differing Sulfur Regimes
title_sort metatranscriptional response of chemoautotrophic ifremeria nautilei endosymbionts to differing sulfur regimes
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4949241/
https://www.ncbi.nlm.nih.gov/pubmed/27486438
http://dx.doi.org/10.3389/fmicb.2016.01074
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