Depth Profile of Nitrifying Archaeal and Bacterial Communities in the Remote Oligotrophic Waters of the North Pacific

Nitrification is a vital ecosystem function in the open ocean that regenerates inorganic nitrogen and promotes primary production. Recent studies have shown that the ecology and physiology of nitrifying organisms is more complex than previously postulated. The distribution of these organisms in the...

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Main Authors: Miguel Semedo, Eva Lopes, Mafalda S. Baptista, Ainhoa Oller-Ruiz, Javier Gilabert, Maria Paola Tomasino, Catarina Magalhães
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.624071/full
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author Miguel Semedo
Eva Lopes
Mafalda S. Baptista
Mafalda S. Baptista
Mafalda S. Baptista
Ainhoa Oller-Ruiz
Javier Gilabert
Maria Paola Tomasino
Catarina Magalhães
Catarina Magalhães
Catarina Magalhães
author_facet Miguel Semedo
Eva Lopes
Mafalda S. Baptista
Mafalda S. Baptista
Mafalda S. Baptista
Ainhoa Oller-Ruiz
Javier Gilabert
Maria Paola Tomasino
Catarina Magalhães
Catarina Magalhães
Catarina Magalhães
author_sort Miguel Semedo
collection DOAJ
description Nitrification is a vital ecosystem function in the open ocean that regenerates inorganic nitrogen and promotes primary production. Recent studies have shown that the ecology and physiology of nitrifying organisms is more complex than previously postulated. The distribution of these organisms in the remote oligotrophic ocean and their interactions with the physicochemical environment are relatively understudied. In this work, we aimed to evaluate the depth profile of nitrifying archaea and bacteria in the Eastern North Pacific Subtropical Front, an area with limited biological surveys but with intense trophic transferences and physicochemical gradients. Furthermore, we investigated the dominant physicochemical and biological relationships within and between ammonia-oxidizing archaea (AOA), ammonia-oxidizing bacteria (AOB), and nitrite-oxidizing bacteria (NOB) as well as with the overall prokaryotic community. We used a 16S rRNA gene sequencing approach to identify and characterize the nitrifying groups within the first 500 m of the water column and to analyze their abiotic and biotic interactions. The water column was characterized mainly by two contrasting environments, warm O2-rich surface waters with low dissolved inorganic nitrogen (DIN) and a cold O2-deficient mesopelagic layer with high concentrations of nitrate (NO3–). Thaumarcheotal AOA and bacterial NOB were highly abundant below the deep chlorophyll maximum (DCM) and in the mesopelagic. In the mesopelagic, AOA and NOB represented up to 25 and 3% of the total prokaryotic community, respectively. Interestingly, the AOA community in the mesopelagic was dominated by unclassified genera that may constitute a novel group of AOA highly adapted to the conditions observed at those depths. Several of these unclassified amplicon sequence variants (ASVs) were positively correlated with NO3– concentrations and negatively correlated with temperature and O2, whereas known thaumarcheotal genera exhibited the opposite behavior. Additionally, we found a large network of positive interactions within and between putative nitrifying ASVs and other prokaryotic groups, including 13230 significant correlations and 23 sub-communities of AOA, AOB, NOB, irrespective of their taxonomic classification. This study provides new insights into our understanding of the roles that AOA may play in recycling inorganic nitrogen in the oligotrophic ocean, with potential consequences to primary production in these remote ecosystems.
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spelling doaj.art-ad59155410824e4ea3bb0775e5eb9e312022-12-21T23:45:53ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-02-011210.3389/fmicb.2021.624071624071Depth Profile of Nitrifying Archaeal and Bacterial Communities in the Remote Oligotrophic Waters of the North PacificMiguel Semedo0Eva Lopes1Mafalda S. Baptista2Mafalda S. Baptista3Mafalda S. Baptista4Ainhoa Oller-Ruiz5Javier Gilabert6Maria Paola Tomasino7Catarina Magalhães8Catarina Magalhães9Catarina Magalhães10Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, Matosinhos, PortugalInterdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, Matosinhos, PortugalInterdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, Matosinhos, PortugalFaculty of Sciences, University of Porto, Porto, PortugalInternational Centre for Terrestrial Antarctic Research, University of Waikato, Hamilton, New ZealandDepartment of Chemical & Environmental Engineering, Universidad Politécnica de Cartagena (UPCT), Cartagena, SpainDepartment of Chemical & Environmental Engineering, Universidad Politécnica de Cartagena (UPCT), Cartagena, SpainInterdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, Matosinhos, PortugalInterdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, Matosinhos, PortugalFaculty of Sciences, University of Porto, Porto, PortugalSchool of Science, Faculty of Science and Engineering, University of Waikato, Hamilton, New ZealandNitrification is a vital ecosystem function in the open ocean that regenerates inorganic nitrogen and promotes primary production. Recent studies have shown that the ecology and physiology of nitrifying organisms is more complex than previously postulated. The distribution of these organisms in the remote oligotrophic ocean and their interactions with the physicochemical environment are relatively understudied. In this work, we aimed to evaluate the depth profile of nitrifying archaea and bacteria in the Eastern North Pacific Subtropical Front, an area with limited biological surveys but with intense trophic transferences and physicochemical gradients. Furthermore, we investigated the dominant physicochemical and biological relationships within and between ammonia-oxidizing archaea (AOA), ammonia-oxidizing bacteria (AOB), and nitrite-oxidizing bacteria (NOB) as well as with the overall prokaryotic community. We used a 16S rRNA gene sequencing approach to identify and characterize the nitrifying groups within the first 500 m of the water column and to analyze their abiotic and biotic interactions. The water column was characterized mainly by two contrasting environments, warm O2-rich surface waters with low dissolved inorganic nitrogen (DIN) and a cold O2-deficient mesopelagic layer with high concentrations of nitrate (NO3–). Thaumarcheotal AOA and bacterial NOB were highly abundant below the deep chlorophyll maximum (DCM) and in the mesopelagic. In the mesopelagic, AOA and NOB represented up to 25 and 3% of the total prokaryotic community, respectively. Interestingly, the AOA community in the mesopelagic was dominated by unclassified genera that may constitute a novel group of AOA highly adapted to the conditions observed at those depths. Several of these unclassified amplicon sequence variants (ASVs) were positively correlated with NO3– concentrations and negatively correlated with temperature and O2, whereas known thaumarcheotal genera exhibited the opposite behavior. Additionally, we found a large network of positive interactions within and between putative nitrifying ASVs and other prokaryotic groups, including 13230 significant correlations and 23 sub-communities of AOA, AOB, NOB, irrespective of their taxonomic classification. This study provides new insights into our understanding of the roles that AOA may play in recycling inorganic nitrogen in the oligotrophic ocean, with potential consequences to primary production in these remote ecosystems.https://www.frontiersin.org/articles/10.3389/fmicb.2021.624071/fullnitrificationthaumarchaeotaAOANOBPacific Subtropical Front
spellingShingle Miguel Semedo
Eva Lopes
Mafalda S. Baptista
Mafalda S. Baptista
Mafalda S. Baptista
Ainhoa Oller-Ruiz
Javier Gilabert
Maria Paola Tomasino
Catarina Magalhães
Catarina Magalhães
Catarina Magalhães
Depth Profile of Nitrifying Archaeal and Bacterial Communities in the Remote Oligotrophic Waters of the North Pacific
Frontiers in Microbiology
nitrification
thaumarchaeota
AOA
NOB
Pacific Subtropical Front
title Depth Profile of Nitrifying Archaeal and Bacterial Communities in the Remote Oligotrophic Waters of the North Pacific
title_full Depth Profile of Nitrifying Archaeal and Bacterial Communities in the Remote Oligotrophic Waters of the North Pacific
title_fullStr Depth Profile of Nitrifying Archaeal and Bacterial Communities in the Remote Oligotrophic Waters of the North Pacific
title_full_unstemmed Depth Profile of Nitrifying Archaeal and Bacterial Communities in the Remote Oligotrophic Waters of the North Pacific
title_short Depth Profile of Nitrifying Archaeal and Bacterial Communities in the Remote Oligotrophic Waters of the North Pacific
title_sort depth profile of nitrifying archaeal and bacterial communities in the remote oligotrophic waters of the north pacific
topic nitrification
thaumarchaeota
AOA
NOB
Pacific Subtropical Front
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.624071/full
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