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Viral Infections Boost Prokaryotic Biomass Production and Organic C Cycling in Hadal Trench Sediments

Hadal trenches are among the most remote and least explored ecosystems on Earth and can support high benthic microbial standing stocks and activities. However, information on the role of viruses in such ecosystems and their interactions with prokaryotic hosts is very limited. Here, we investigated a...

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Autores principales: Manea, Elisabetta, Dell’Anno, Antonio, Rastelli, Eugenio, Tangherlini, Michael, Nunoura, Takuro, Nomaki, Hidetaka, Danovaro, Roberto, Corinaldesi, Cinzia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6716271/
https://www.ncbi.nlm.nih.gov/pubmed/31507564
http://dx.doi.org/10.3389/fmicb.2019.01952
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author Manea, Elisabetta
Dell’Anno, Antonio
Rastelli, Eugenio
Tangherlini, Michael
Nunoura, Takuro
Nomaki, Hidetaka
Danovaro, Roberto
Corinaldesi, Cinzia
author_facet Manea, Elisabetta
Dell’Anno, Antonio
Rastelli, Eugenio
Tangherlini, Michael
Nunoura, Takuro
Nomaki, Hidetaka
Danovaro, Roberto
Corinaldesi, Cinzia
author_sort Manea, Elisabetta
collection PubMed
description Hadal trenches are among the most remote and least explored ecosystems on Earth and can support high benthic microbial standing stocks and activities. However, information on the role of viruses in such ecosystems and their interactions with prokaryotic hosts is very limited. Here, we investigated activities of benthic viruses and prokaryotes and their interactions in three hadal trenches (Japan, Izu-Ogasawara and Mariana trenches) and in their nearby abyssal sites. Our findings reveal that these hadal trenches, compared with the surrounding abyssal sites, support higher abundances and biomasses of prokaryotes. In addition, the high prokaryotic biomasses of hadal trenches could favor high rates of viral infection and cell lysis, especially in the Japan Trench. Hadal viruses can release large amounts of highly labile and promptly available organic material by inducing cell lysis, which could contribute to sustain benthic prokaryotes and decrease their dependency on the enzymatic digestion of the more refractory fraction of sediment organic matter. Our results suggest that this process can contribute to explain the discrepancy between high prokaryote biomass and apparent low efficiency in the utilization of the sedimentary organic matter in the hadal ecosystems. Concluding, hadal trenches may be characterized by a highly dynamic viral component, which can boost prokaryotic biomass production, thereby profoundly influencing the functioning of these remote and extreme ecosystems.
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spelling pubmed-67162712019-09-10 Viral Infections Boost Prokaryotic Biomass Production and Organic C Cycling in Hadal Trench Sediments Manea, Elisabetta Dell’Anno, Antonio Rastelli, Eugenio Tangherlini, Michael Nunoura, Takuro Nomaki, Hidetaka Danovaro, Roberto Corinaldesi, Cinzia Front Microbiol Microbiology Hadal trenches are among the most remote and least explored ecosystems on Earth and can support high benthic microbial standing stocks and activities. However, information on the role of viruses in such ecosystems and their interactions with prokaryotic hosts is very limited. Here, we investigated activities of benthic viruses and prokaryotes and their interactions in three hadal trenches (Japan, Izu-Ogasawara and Mariana trenches) and in their nearby abyssal sites. Our findings reveal that these hadal trenches, compared with the surrounding abyssal sites, support higher abundances and biomasses of prokaryotes. In addition, the high prokaryotic biomasses of hadal trenches could favor high rates of viral infection and cell lysis, especially in the Japan Trench. Hadal viruses can release large amounts of highly labile and promptly available organic material by inducing cell lysis, which could contribute to sustain benthic prokaryotes and decrease their dependency on the enzymatic digestion of the more refractory fraction of sediment organic matter. Our results suggest that this process can contribute to explain the discrepancy between high prokaryote biomass and apparent low efficiency in the utilization of the sedimentary organic matter in the hadal ecosystems. Concluding, hadal trenches may be characterized by a highly dynamic viral component, which can boost prokaryotic biomass production, thereby profoundly influencing the functioning of these remote and extreme ecosystems. Frontiers Media S.A. 2019-08-23 /pmc/articles/PMC6716271/ /pubmed/31507564 http://dx.doi.org/10.3389/fmicb.2019.01952 Text en Copyright © 2019 Manea, Dell’Anno, Rastelli, Tangherlini, Nunoura, Nomaki, Danovaro and Corinaldesi. 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) and the copyright owner(s) 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
Manea, Elisabetta
Dell’Anno, Antonio
Rastelli, Eugenio
Tangherlini, Michael
Nunoura, Takuro
Nomaki, Hidetaka
Danovaro, Roberto
Corinaldesi, Cinzia
Viral Infections Boost Prokaryotic Biomass Production and Organic C Cycling in Hadal Trench Sediments
title Viral Infections Boost Prokaryotic Biomass Production and Organic C Cycling in Hadal Trench Sediments
title_full Viral Infections Boost Prokaryotic Biomass Production and Organic C Cycling in Hadal Trench Sediments
title_fullStr Viral Infections Boost Prokaryotic Biomass Production and Organic C Cycling in Hadal Trench Sediments
title_full_unstemmed Viral Infections Boost Prokaryotic Biomass Production and Organic C Cycling in Hadal Trench Sediments
title_short Viral Infections Boost Prokaryotic Biomass Production and Organic C Cycling in Hadal Trench Sediments
title_sort viral infections boost prokaryotic biomass production and organic c cycling in hadal trench sediments
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6716271/
https://www.ncbi.nlm.nih.gov/pubmed/31507564
http://dx.doi.org/10.3389/fmicb.2019.01952
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