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Reconstructing the Genetic Potential of the Microbially-Mediated Nitrogen Cycle in a Salt Marsh Ecosystem

Coastal ecosystems are considered buffer zones for the discharge of land-derived nutrients without accounting for potential negative side effects. Hence, there is an urgent need to better understand the ecological assembly and dynamics of the microorganisms that are involved in nitrogen (N) cycling...

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Autores principales: Dini-Andreote, Francisco, Brossi, Maria Julia de L., van Elsas, Jan Dirk, Salles, Joana F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4908922/
https://www.ncbi.nlm.nih.gov/pubmed/27379042
http://dx.doi.org/10.3389/fmicb.2016.00902
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author Dini-Andreote, Francisco
Brossi, Maria Julia de L.
van Elsas, Jan Dirk
Salles, Joana F.
author_facet Dini-Andreote, Francisco
Brossi, Maria Julia de L.
van Elsas, Jan Dirk
Salles, Joana F.
author_sort Dini-Andreote, Francisco
collection PubMed
description Coastal ecosystems are considered buffer zones for the discharge of land-derived nutrients without accounting for potential negative side effects. Hence, there is an urgent need to better understand the ecological assembly and dynamics of the microorganisms that are involved in nitrogen (N) cycling in such systems. Here, we employed two complementary methodological approaches (i.e., shotgun metagenomics and quantitative PCR) to examine the distribution and abundance of selected microbial genes involved in N transformations. We used soil samples collected along a well-established pristine salt marsh soil chronosequence that spans over a century of ecosystem development at the island of Schiermonnikoog, The Netherlands. Across the examined soil successional stages, the structure of the populations of genes involved in N cycling processes was strongly related to (shifts in the) soil nitrogen levels (i.e., [Formula: see text] , [Formula: see text]), salinity and pH (explaining 73.8% of the total variation, R(2) = 0.71). Quantification of the genes used as proxies for N fixation, nitrification and denitrification revealed clear successional signatures that corroborated the taxonomic assignments obtained by metagenomics. Notably, we found strong evidence for niche partitioning, as revealed by the abundance and distribution of marker genes for nitrification (ammonia-oxidizing bacteria and archaea) and denitrification (nitrite reductase nirK, nirS and nitrous oxide reductase nosZ clades I and II). This was supported by a distinct correlation between these genes and soil physico-chemical properties, such as soil physical structure, pH, salinity, organic matter, total N, [Formula: see text] , [Formula: see text] and [Formula: see text] , across four seasonal samplings. Overall, this study sheds light on the successional trajectories of microbial N cycle genes along a naturally developing salt marsh ecosystem. The data obtained serve as a foundation to guide the formulation of ecological models that aim to effectively monitor and manage pristine and impacted salt marsh areas. Such models should account for the ecology as well as the historical contingency of N cycling communities.
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spelling pubmed-49089222016-07-04 Reconstructing the Genetic Potential of the Microbially-Mediated Nitrogen Cycle in a Salt Marsh Ecosystem Dini-Andreote, Francisco Brossi, Maria Julia de L. van Elsas, Jan Dirk Salles, Joana F. Front Microbiol Microbiology Coastal ecosystems are considered buffer zones for the discharge of land-derived nutrients without accounting for potential negative side effects. Hence, there is an urgent need to better understand the ecological assembly and dynamics of the microorganisms that are involved in nitrogen (N) cycling in such systems. Here, we employed two complementary methodological approaches (i.e., shotgun metagenomics and quantitative PCR) to examine the distribution and abundance of selected microbial genes involved in N transformations. We used soil samples collected along a well-established pristine salt marsh soil chronosequence that spans over a century of ecosystem development at the island of Schiermonnikoog, The Netherlands. Across the examined soil successional stages, the structure of the populations of genes involved in N cycling processes was strongly related to (shifts in the) soil nitrogen levels (i.e., [Formula: see text] , [Formula: see text]), salinity and pH (explaining 73.8% of the total variation, R(2) = 0.71). Quantification of the genes used as proxies for N fixation, nitrification and denitrification revealed clear successional signatures that corroborated the taxonomic assignments obtained by metagenomics. Notably, we found strong evidence for niche partitioning, as revealed by the abundance and distribution of marker genes for nitrification (ammonia-oxidizing bacteria and archaea) and denitrification (nitrite reductase nirK, nirS and nitrous oxide reductase nosZ clades I and II). This was supported by a distinct correlation between these genes and soil physico-chemical properties, such as soil physical structure, pH, salinity, organic matter, total N, [Formula: see text] , [Formula: see text] and [Formula: see text] , across four seasonal samplings. Overall, this study sheds light on the successional trajectories of microbial N cycle genes along a naturally developing salt marsh ecosystem. The data obtained serve as a foundation to guide the formulation of ecological models that aim to effectively monitor and manage pristine and impacted salt marsh areas. Such models should account for the ecology as well as the historical contingency of N cycling communities. Frontiers Media S.A. 2016-06-15 /pmc/articles/PMC4908922/ /pubmed/27379042 http://dx.doi.org/10.3389/fmicb.2016.00902 Text en Copyright © 2016 Dini-Andreote, Brossi, van Elsas and Salles. 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
Dini-Andreote, Francisco
Brossi, Maria Julia de L.
van Elsas, Jan Dirk
Salles, Joana F.
Reconstructing the Genetic Potential of the Microbially-Mediated Nitrogen Cycle in a Salt Marsh Ecosystem
title Reconstructing the Genetic Potential of the Microbially-Mediated Nitrogen Cycle in a Salt Marsh Ecosystem
title_full Reconstructing the Genetic Potential of the Microbially-Mediated Nitrogen Cycle in a Salt Marsh Ecosystem
title_fullStr Reconstructing the Genetic Potential of the Microbially-Mediated Nitrogen Cycle in a Salt Marsh Ecosystem
title_full_unstemmed Reconstructing the Genetic Potential of the Microbially-Mediated Nitrogen Cycle in a Salt Marsh Ecosystem
title_short Reconstructing the Genetic Potential of the Microbially-Mediated Nitrogen Cycle in a Salt Marsh Ecosystem
title_sort reconstructing the genetic potential of the microbially-mediated nitrogen cycle in a salt marsh ecosystem
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4908922/
https://www.ncbi.nlm.nih.gov/pubmed/27379042
http://dx.doi.org/10.3389/fmicb.2016.00902
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