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The Link between Microbial Diversity and Nitrogen Cycling in Marine Sediments Is Modulated by Macrofaunal Bioturbation

OBJECTIVES: The marine benthic nitrogen cycle is affected by both the presence and activity of macrofauna and the diversity of N-cycling microbes. However, integrated research simultaneously investigating macrofauna, microbes and N-cycling is lacking. We investigated spatio-temporal patterns in micr...

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Autores principales: Yazdani Foshtomi, Maryam, Braeckman, Ulrike, Derycke, Sofie, Sapp, Melanie, Van Gansbeke, Dirk, Sabbe, Koen, Willems, Anne, Vincx, Magda, Vanaverbeke, Jan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4477903/
https://www.ncbi.nlm.nih.gov/pubmed/26102286
http://dx.doi.org/10.1371/journal.pone.0130116
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author Yazdani Foshtomi, Maryam
Braeckman, Ulrike
Derycke, Sofie
Sapp, Melanie
Van Gansbeke, Dirk
Sabbe, Koen
Willems, Anne
Vincx, Magda
Vanaverbeke, Jan
author_facet Yazdani Foshtomi, Maryam
Braeckman, Ulrike
Derycke, Sofie
Sapp, Melanie
Van Gansbeke, Dirk
Sabbe, Koen
Willems, Anne
Vincx, Magda
Vanaverbeke, Jan
author_sort Yazdani Foshtomi, Maryam
collection PubMed
description OBJECTIVES: The marine benthic nitrogen cycle is affected by both the presence and activity of macrofauna and the diversity of N-cycling microbes. However, integrated research simultaneously investigating macrofauna, microbes and N-cycling is lacking. We investigated spatio-temporal patterns in microbial community composition and diversity, macrofaunal abundance and their sediment reworking activity, and N-cycling in seven subtidal stations in the Southern North Sea. SPATIO-TEMPORAL PATTERNS OF THE MICROBIAL COMMUNITIES: Our results indicated that bacteria (total and β-AOB) showed more spatio-temporal variation than archaea (total and AOA) as sedimentation of organic matter and the subsequent changes in the environment had a stronger impact on their community composition and diversity indices in our study area. However, spatio-temporal patterns of total bacterial and β-AOB communities were different and related to the availability of ammonium for the autotrophic β-AOB. Highest bacterial richness and diversity were observed in June at the timing of the phytoplankton bloom deposition, while richness of β-AOB as well as AOA peaked in September. Total archaeal community showed no temporal variation in diversity indices. MACROFAUNA, MICROBES AND THE BENTHIC N-CYCLE: Distance based linear models revealed that, independent from the effect of grain size and the quality and quantity of sediment organic matter, nitrification and N-mineralization were affected by respectively the diversity of metabolically active β-AOB and AOA, and the total bacteria, near the sediment-water interface. Separate models demonstrated a significant and independent effect of macrofaunal activities on community composition and richness of total bacteria, and diversity indices of metabolically active AOA. Diversity of β-AOB was significantly affected by macrofaunal abundance. Our results support the link between microbial biodiversity and ecosystem functioning in marine sediments, and provided broad correlative support for the hypothesis that this relationship is modulated by macrofaunal activity. We hypothesized that the latter effect can be explained by their bioturbating and bio-irrigating activities, increasing the spatial complexity of the biogeochemical environment.
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spelling pubmed-44779032015-07-02 The Link between Microbial Diversity and Nitrogen Cycling in Marine Sediments Is Modulated by Macrofaunal Bioturbation Yazdani Foshtomi, Maryam Braeckman, Ulrike Derycke, Sofie Sapp, Melanie Van Gansbeke, Dirk Sabbe, Koen Willems, Anne Vincx, Magda Vanaverbeke, Jan PLoS One Research Article OBJECTIVES: The marine benthic nitrogen cycle is affected by both the presence and activity of macrofauna and the diversity of N-cycling microbes. However, integrated research simultaneously investigating macrofauna, microbes and N-cycling is lacking. We investigated spatio-temporal patterns in microbial community composition and diversity, macrofaunal abundance and their sediment reworking activity, and N-cycling in seven subtidal stations in the Southern North Sea. SPATIO-TEMPORAL PATTERNS OF THE MICROBIAL COMMUNITIES: Our results indicated that bacteria (total and β-AOB) showed more spatio-temporal variation than archaea (total and AOA) as sedimentation of organic matter and the subsequent changes in the environment had a stronger impact on their community composition and diversity indices in our study area. However, spatio-temporal patterns of total bacterial and β-AOB communities were different and related to the availability of ammonium for the autotrophic β-AOB. Highest bacterial richness and diversity were observed in June at the timing of the phytoplankton bloom deposition, while richness of β-AOB as well as AOA peaked in September. Total archaeal community showed no temporal variation in diversity indices. MACROFAUNA, MICROBES AND THE BENTHIC N-CYCLE: Distance based linear models revealed that, independent from the effect of grain size and the quality and quantity of sediment organic matter, nitrification and N-mineralization were affected by respectively the diversity of metabolically active β-AOB and AOA, and the total bacteria, near the sediment-water interface. Separate models demonstrated a significant and independent effect of macrofaunal activities on community composition and richness of total bacteria, and diversity indices of metabolically active AOA. Diversity of β-AOB was significantly affected by macrofaunal abundance. Our results support the link between microbial biodiversity and ecosystem functioning in marine sediments, and provided broad correlative support for the hypothesis that this relationship is modulated by macrofaunal activity. We hypothesized that the latter effect can be explained by their bioturbating and bio-irrigating activities, increasing the spatial complexity of the biogeochemical environment. Public Library of Science 2015-06-23 /pmc/articles/PMC4477903/ /pubmed/26102286 http://dx.doi.org/10.1371/journal.pone.0130116 Text en © 2015 Yazdani Foshtomi et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Yazdani Foshtomi, Maryam
Braeckman, Ulrike
Derycke, Sofie
Sapp, Melanie
Van Gansbeke, Dirk
Sabbe, Koen
Willems, Anne
Vincx, Magda
Vanaverbeke, Jan
The Link between Microbial Diversity and Nitrogen Cycling in Marine Sediments Is Modulated by Macrofaunal Bioturbation
title The Link between Microbial Diversity and Nitrogen Cycling in Marine Sediments Is Modulated by Macrofaunal Bioturbation
title_full The Link between Microbial Diversity and Nitrogen Cycling in Marine Sediments Is Modulated by Macrofaunal Bioturbation
title_fullStr The Link between Microbial Diversity and Nitrogen Cycling in Marine Sediments Is Modulated by Macrofaunal Bioturbation
title_full_unstemmed The Link between Microbial Diversity and Nitrogen Cycling in Marine Sediments Is Modulated by Macrofaunal Bioturbation
title_short The Link between Microbial Diversity and Nitrogen Cycling in Marine Sediments Is Modulated by Macrofaunal Bioturbation
title_sort link between microbial diversity and nitrogen cycling in marine sediments is modulated by macrofaunal bioturbation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4477903/
https://www.ncbi.nlm.nih.gov/pubmed/26102286
http://dx.doi.org/10.1371/journal.pone.0130116
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