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Abstract Ammonia-oxidizing archaea (AOA) are among the most abundant and ubiquitous microorganisms in the ocean, exerting primary control on nitrification and nitrogen oxides emission. Although united by a common physiology of chemoautotrophic growth on ammonia, a corresponding high genomic and habitat variability suggests tremendous adaptive capacity. Here, we compared 44 diverse AOA genomes, 37 from species cultivated from samples collected across diverse geographic locations and seven assembled from metagenomic sequences from the mesopelagic to hadopelagic zones of the deep ocean. Comparative analysis identified seven major marine AOA genotypic groups having gene content correlated with their distinctive biogeographies. Phosphorus and ammonia availabilities as well as hydrostatic pressure were identified as selective forces driving marine AOA genotypic and gene content variability in different oceanic regions. Notably, AOA methylphosphonate biosynthetic genes span diverse oceanic provinces, reinforcing their importance for methane production in the ocean. Together, our combined comparative physiological, genomic, and metagenomic analyses provide a comprehensive view of the biogeography of globally abundant AOA and their adaptive radiation into a vast range of marine and terrestrial habitats.
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Heterotrophic Thaumarchaea with Small Genomes Are Widespread in the Dark Ocean
ABSTRACT The Thaumarchaeota is a diverse archaeal phylum comprising numerous lineages that play key roles in global biogeochemical cycling, particularly in the ocean. To date, all genomically characterized marine thaumarchaea are reported to be chemolithoautotrophic ammonia oxidizers. In this study, we report a group of putatively heterotrophic marine thaumarchaea (HMT) with small genome sizes that is globally abundant in the mesopelagic, apparently lacking the ability to oxidize ammonia. We assembled five HMT genomes from metagenomic data and show that they form a deeply branching sister lineage to the ammonia-oxidizing archaea (AOA). We identify this group in metagenomes from mesopelagic waters in all major ocean basins, with abundances reaching up to 6% of that of AOA. Surprisingly, we predict the HMT have small genomes of ∼1 Mbp, and our ancestral state reconstruction indicates this lineage has undergone substantial genome reduction compared to other related archaea. The genomic repertoire of HMT indicates a versatile metabolism for aerobic chemoorganoheterotrophy that includes a divergent form III-a RuBisCO, a 2M respiratory complex I that has been hypothesized to increase energetic efficiency, and a three-subunit heme-copper oxidase complex IV that is absent from AOA. We also identify 21 pyrroloquinoline quinone (PQQ)-dependent dehydrogenases that are predicted to supply reducing equivalents to the electron transport chain and are among the most highly expressed HMT genes, suggesting these enzymes play an important role in the physiology of this group. Our results suggest that heterotrophic members of the Thaumarchaeota are widespread in the ocean and potentially play key roles in global chemical transformations. IMPORTANCE It has been known for many years that marine Thaumarchaeota are abundant constituents of dark ocean microbial communities, where their ability to couple ammonia oxidation and carbon fixation plays a critical role in nutrient dynamics. In this study, we describe an abundant group of putatively heterotrophic marine Thaumarchaeota (HMT) in the ocean with physiology distinct from those of their ammonia-oxidizing relatives. HMT lack the ability to oxidize ammonia and fix carbon via the 3-hydroxypropionate/4-hydroxybutyrate pathway but instead encode a form III-a RuBisCO and diverse PQQ-dependent dehydrogenases that are likely used to conserve energy in the dark ocean. Our work expands the scope of known diversity of Thaumarchaeota in the ocean and provides important insight into a widespread marine lineage.
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- Award ID(s):
- 1918271
- PAR ID:
- 10166975
- Date Published:
- Journal Name:
- mSystems
- Volume:
- 5
- Issue:
- 3
- ISSN:
- 2379-5077
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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ABSTRACT: Nitrification is a globally important biogeochemical process, helping to remove excess nitrogen from the biosphere. Thaumarchaeota are important contributors to ammonium oxidation, the first step in nitrification, especially in the ocean. A phylogenetic distinction between clades of marine Thaumarchaeota from shallow versus mesopelagic habitats emerged from the earliest analyses of sequence databases, yet the environmental factors driving these distributions, and their biogeochemical significance, are still debated. Steady-state ammonium concentrations are important determinants; however, environmental concentrations may fluctuate on short time scales, depending on localized coupling between production and consumption. Substrate pulses have been shown to inhibit the activity of Thaumarchaeota cultures via the accumulation of toxic intermediates. Evidence from experiments performed with samples from the Southern Ocean off the West Antarctic Peninsula show that ammonia oxidation can be strongly inhibited by ammonium amendments. We found greater inhibition with mesopelagic samples than with those from shallower water. Pulses of urea also inhibited the oxidation of urea-N, but to a lesser extent than ammonium pulses affected ammonia oxidation. The inhibition also affects carbon fixation, which may thus be greater in the dark ocean than currently believed. The differential response of meso- versus epipelagic Thaumarchaeota populations to pulses of ammonium potentially explains the evolutionary divergence of marine Thaumarchaeota into deep- and shallow-water clades. Measurements of ammonium oxidation rates needed for biogeochemical models are typically made with substrate amendments that may yield artificially low rates, to 25% of the uninhibited rate, in mesopelagic samples.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1128/mSystems.00415-20
