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Ammonia-oxidizing archaea have similar power requirements in diverse marine oxic sediments.

ABSTRACT: Energy/power availability is regarded as one of the ultimate controlling factors of microbial abundance in the deep biosphere, where fewer cells are found in habitats of lower energy availability. A critical assumption driving the proportional relationship between total cell abundance and power availability is that the cell-specific power requirement keeps constant or varies over smaller ranges than other variables, which has yet to be validated. Here we present a quantitative framework to determine the cell-specific power requirement of the omnipresent ammonia-oxidizing archaea (AOA) in eight sediment cores with 3-4 orders of magnitude variations of organic matter flux and oxygen penetration depth. Our results show that despite the six orders of magnitude variations in the rates and power supply of nitrification and AOA abundances across these eight cores, the cell-specific power requirement of AOA from different cores and depths overlaps within the narrow range of 10^-19-10^-17 W cell^-1, where the lower end may represent the basal power requirement of microorganisms persisting in subseafloor sediments. In individual cores, AOA also exhibit similar cell-specific power requirements, regardless of the AOA population size or sediment depth/age. Such quantitative insights establish a relationship between the power supply and the total abundance of AOA, and therefore lay a foundation for a first-order estimate of the standing stock of AOA in global marine oxic sediments.

SUBMITTER: Zhao R

PROVIDER: S-EPMC8630020 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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.

Project description:The potential for oxidation of ammonia in anoxic marine sediments exists through anaerobic oxidation by Nitrosomonas-like organisms, utilizing nitrogen dioxide, coupling of nitrification, manganese reduction, and anaerobic oxidation of ammonium by planctomycetes (the Anammox process). Here we describe the presence of microbial communities with the potential to carry out these processes in a natural marine sediment system (Loch Duich, Scotland). Natural microbial communities of Planctomycetales-Verrucomicrobia and beta- and gamma-proteobacterial ammonia-oxidizing bacteria were characterized by analysis of 16S rRNA genes amplified using group-specific primers by PCR- and reverse transcription-PCR amplification of 16S rDNA and RNA, respectively. Amplification products were analyzed by sequencing of clones and by denaturant gradient gel electrophoresis (DGGE). Amplification of primers specific for Planctomycetales-Verrucomicrobia and beta-proteobacterial ammonia-oxidizing bacteria generated products at all sampling sites and depths, but no product was generated using primers specific for gamma-proteobacterial ammonia-oxidizing bacteria. 16S rDNA DGGE banding patterns indicated complex communities of beta-proteobacterial ammonia-oxidizing bacteria in anoxic marine sediments. Phylogenetic analysis of sequences from clones and those excised from DGGE gels suggests dominance of Nitrosospira cluster 1-like organisms and of strains belonging to a novel cluster represented in dominant bands in 16S rRNA DGGE banding patterns. Their presence indicates a group of organisms closely related to recognized beta-proteobacterial ammonia-oxidizing bacteria that may be selected in anoxic environments and may be capable of anoxic ammonia oxidation. Sequence analysis of planctomycete clone libraries and sequences excised from DGGE gels also demonstrated a diverse microbial community and suggested the presence of new subdivisions, but no sequence related to recognized Anammox organisms was detected.

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Ammonia-oxidizing archaea have similar power requirements in diverse marine oxic sediments.

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