Indigenous Ammonia-Oxidizing Archaea in Oxic Subseafloor Oceanic Crust

ABSTRACT Oceanic ridge flank systems represent one of the largest and least-explored microbial habitats on Earth. Fundamental ecological questions regarding community activity, recruitment, and succession in this environment remain unanswered. Here, we investigated ammonia-oxidizing archaea (AOA) in...

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Autores principales:	Rui Zhao, Håkon Dahle, Gustavo A. Ramírez, Steffen L. Jørgensen
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	nitrification Thaumarchaeota deep biosphere oceanic crust Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/346ec85196b444b29e8a005c078358ca
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spelling	oai:doaj.org-article:346ec85196b444b29e8a005c078358ca2021-12-02T18:44:38ZIndigenous Ammonia-Oxidizing Archaea in Oxic Subseafloor Oceanic Crust10.1128/mSystems.00758-192379-5077https://doaj.org/article/346ec85196b444b29e8a005c078358ca2020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00758-19https://doaj.org/toc/2379-5077ABSTRACT Oceanic ridge flank systems represent one of the largest and least-explored microbial habitats on Earth. Fundamental ecological questions regarding community activity, recruitment, and succession in this environment remain unanswered. Here, we investigated ammonia-oxidizing archaea (AOA) in the sediment-buried basalts on the oxic and young ridge flank at North Pond, a sediment-filled pond on the western flank of the Mid-Atlantic Ridge, and compared them with those in the overlying sediments and bottom seawater. Nitrification in the North Pond basement is thermodynamically favorable and is supported by a reaction-transport model simulating the dynamics of nitrate in the crustal fluids. Nitrification rate is estimated to account for 6% to 7% of oxygen consumption, which is similar to the ratios found in marine oxic sediments, suggesting that aerobic mineralization of organic matter is the major ammonium source for crustal nitrifiers. Using the archaeal 16S rRNA and amoA genes as phylogenetic markers, we show that AOA, composed solely of Nitrosopumilaceae, are the major archaeal dwellers at North Pond. Phylogenetic analysis reveals that the crustal AOA communities are distinct from those in the bottom seawater and the upper oxic sediments but are similar to those in the basal part of the overlying sediment column, suggesting either similar environmental selection or the dispersal of microbes across the sediment-basement interface. Additionally, quantitative abundance data suggest enrichment of the dominant Nitrosopumilaceae clade (Eta clade) in the basement compared to the seawater. This study explored AOA and their activity in the upper oceanic crust, and our results have ecological implications for the biogeochemical cycling of nitrogen in the crustal subsurface. IMPORTANCE Ridge flanks represent the major avenue of chemical and heat exchange between the Earth’s oceans and the lithosphere and are thought to harbor an enormous and understudied biosphere. However, little is known about the diversity and functionality of the crustal biosphere. Here, we report an indigenous community of archaea specialized in ammonia oxidation (i.e., AOA) in the oxic oceanic crust at North Pond. These AOA are the dominant archaea and are likely responsible for most of the cycling taking place in the first step of nitrification, a feasible nitrogen cycling step in the oxic basement. The crustal AOA community structure significantly differs from that in deep ocean water but is similar to that of the community in the overlying sediments in close proximity. This report links the occurrence of AOA to their metabolic activity in the oxic subseafloor crust and suggests that ecological selection and in situ proliferation may shape the microbial community structure in the rocky subsurface.Rui ZhaoHåkon DahleGustavo A. RamírezSteffen L. JørgensenAmerican Society for MicrobiologyarticlenitrificationThaumarchaeotadeep biosphereoceanic crustMicrobiologyQR1-502ENmSystems, Vol 5, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	nitrification Thaumarchaeota deep biosphere oceanic crust Microbiology QR1-502
spellingShingle	nitrification Thaumarchaeota deep biosphere oceanic crust Microbiology QR1-502 Rui Zhao Håkon Dahle Gustavo A. Ramírez Steffen L. Jørgensen Indigenous Ammonia-Oxidizing Archaea in Oxic Subseafloor Oceanic Crust
description	ABSTRACT Oceanic ridge flank systems represent one of the largest and least-explored microbial habitats on Earth. Fundamental ecological questions regarding community activity, recruitment, and succession in this environment remain unanswered. Here, we investigated ammonia-oxidizing archaea (AOA) in the sediment-buried basalts on the oxic and young ridge flank at North Pond, a sediment-filled pond on the western flank of the Mid-Atlantic Ridge, and compared them with those in the overlying sediments and bottom seawater. Nitrification in the North Pond basement is thermodynamically favorable and is supported by a reaction-transport model simulating the dynamics of nitrate in the crustal fluids. Nitrification rate is estimated to account for 6% to 7% of oxygen consumption, which is similar to the ratios found in marine oxic sediments, suggesting that aerobic mineralization of organic matter is the major ammonium source for crustal nitrifiers. Using the archaeal 16S rRNA and amoA genes as phylogenetic markers, we show that AOA, composed solely of Nitrosopumilaceae, are the major archaeal dwellers at North Pond. Phylogenetic analysis reveals that the crustal AOA communities are distinct from those in the bottom seawater and the upper oxic sediments but are similar to those in the basal part of the overlying sediment column, suggesting either similar environmental selection or the dispersal of microbes across the sediment-basement interface. Additionally, quantitative abundance data suggest enrichment of the dominant Nitrosopumilaceae clade (Eta clade) in the basement compared to the seawater. This study explored AOA and their activity in the upper oceanic crust, and our results have ecological implications for the biogeochemical cycling of nitrogen in the crustal subsurface. IMPORTANCE Ridge flanks represent the major avenue of chemical and heat exchange between the Earth’s oceans and the lithosphere and are thought to harbor an enormous and understudied biosphere. However, little is known about the diversity and functionality of the crustal biosphere. Here, we report an indigenous community of archaea specialized in ammonia oxidation (i.e., AOA) in the oxic oceanic crust at North Pond. These AOA are the dominant archaea and are likely responsible for most of the cycling taking place in the first step of nitrification, a feasible nitrogen cycling step in the oxic basement. The crustal AOA community structure significantly differs from that in deep ocean water but is similar to that of the community in the overlying sediments in close proximity. This report links the occurrence of AOA to their metabolic activity in the oxic subseafloor crust and suggests that ecological selection and in situ proliferation may shape the microbial community structure in the rocky subsurface.
format	article
author	Rui Zhao Håkon Dahle Gustavo A. Ramírez Steffen L. Jørgensen
author_facet	Rui Zhao Håkon Dahle Gustavo A. Ramírez Steffen L. Jørgensen
author_sort	Rui Zhao
title	Indigenous Ammonia-Oxidizing Archaea in Oxic Subseafloor Oceanic Crust
title_short	Indigenous Ammonia-Oxidizing Archaea in Oxic Subseafloor Oceanic Crust
title_full	Indigenous Ammonia-Oxidizing Archaea in Oxic Subseafloor Oceanic Crust
title_fullStr	Indigenous Ammonia-Oxidizing Archaea in Oxic Subseafloor Oceanic Crust
title_full_unstemmed	Indigenous Ammonia-Oxidizing Archaea in Oxic Subseafloor Oceanic Crust
title_sort	indigenous ammonia-oxidizing archaea in oxic subseafloor oceanic crust
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/346ec85196b444b29e8a005c078358ca
work_keys_str_mv	AT ruizhao indigenousammoniaoxidizingarchaeainoxicsubseaflooroceaniccrust AT hakondahle indigenousammoniaoxidizingarchaeainoxicsubseaflooroceaniccrust AT gustavoaramirez indigenousammoniaoxidizingarchaeainoxicsubseaflooroceaniccrust AT steffenljørgensen indigenousammoniaoxidizingarchaeainoxicsubseaflooroceaniccrust
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Indigenous Ammonia-Oxidizing Archaea in Oxic Subseafloor Oceanic Crust

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