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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Main Authors: Elisabetta Manea, Antonio Dell’Anno, Eugenio Rastelli, Michael Tangherlini, Takuro Nunoura, Hidetaka Nomaki, Roberto Danovaro, Cinzia Corinaldesi
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-08-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.01952/full
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spelling doaj-608a4053690c497f871866a54a7954732020-11-25T01:02:43ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-08-011010.3389/fmicb.2019.01952459069Viral Infections Boost Prokaryotic Biomass Production and Organic C Cycling in Hadal Trench SedimentsElisabetta Manea0Antonio Dell’Anno1Eugenio Rastelli2Michael Tangherlini3Takuro Nunoura4Hidetaka Nomaki5Roberto Danovaro6Roberto Danovaro7Cinzia Corinaldesi8Department of Life and Environmental Sciences, Polytechnic University of Marche, Ancona, ItalyDepartment of Life and Environmental Sciences, Polytechnic University of Marche, Ancona, ItalyStazione Zoologica Anton Dohrn, Naples, ItalyStazione Zoologica Anton Dohrn, Naples, ItalyResearch Center for Bioscience and Nanoscience (CeBN), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, JapanInstitute for Extra-Cutting-Edge Science and Technology Avant-Garde Research (X-star), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, JapanDepartment of Life and Environmental Sciences, Polytechnic University of Marche, Ancona, ItalyStazione Zoologica Anton Dohrn, Naples, ItalyDepartment of Sciences and Engineering of Materials, Environment and Urbanistics, Polytechnic University of Marche, Ancona, ItalyHadal 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.https://www.frontiersin.org/article/10.3389/fmicb.2019.01952/fullhadal trenchesvirusesviral lysisdeep-sea ecosystemsbenthic prokaryotes
collection DOAJ
language English
format Article
sources DOAJ
author Elisabetta Manea
Antonio Dell’Anno
Eugenio Rastelli
Michael Tangherlini
Takuro Nunoura
Hidetaka Nomaki
Roberto Danovaro
Roberto Danovaro
Cinzia Corinaldesi
spellingShingle Elisabetta Manea
Antonio Dell’Anno
Eugenio Rastelli
Michael Tangherlini
Takuro Nunoura
Hidetaka Nomaki
Roberto Danovaro
Roberto Danovaro
Cinzia Corinaldesi
Viral Infections Boost Prokaryotic Biomass Production and Organic C Cycling in Hadal Trench Sediments
Frontiers in Microbiology
hadal trenches
viruses
viral lysis
deep-sea ecosystems
benthic prokaryotes
author_facet Elisabetta Manea
Antonio Dell’Anno
Eugenio Rastelli
Michael Tangherlini
Takuro Nunoura
Hidetaka Nomaki
Roberto Danovaro
Roberto Danovaro
Cinzia Corinaldesi
author_sort Elisabetta Manea
title 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_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_sort viral infections boost prokaryotic biomass production and organic c cycling in hadal trench sediments
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2019-08-01
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.
topic hadal trenches
viruses
viral lysis
deep-sea ecosystems
benthic prokaryotes
url https://www.frontiersin.org/article/10.3389/fmicb.2019.01952/full
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