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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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The Predominance of Ammonia-Oxidizing Archaea in an Oceanic Microbial Community Amended with Cyanobacterial Lysate
ABSTRACT When the oligotrophic microbial community was amended with Synechococcus -derived dissolved organic matter (SDOM) and incubated under the dark condition, archaea relative abundance was initially very low but made up more than 60% of the prokaryotic community on day 60, and remained dominant for at least 9 months. The archaeal sequences were dominated by Candidatus Nitrosopumilus , the Group I.1a Thaumarchaeota. The increase of Thaumarchaeota in the dark incubation corresponded to the period of delayed ammonium oxidation upon an initially steady increase in ammonia, supporting the remarkable competency of Thaumarchaeota in energy utilization and fixation of inorganic carbon in the ocean. IMPORTANCE Thaumarchaeota, which are ammonia-oxidizing archaea (AOA), are mainly chemolithoautotrophs that can fix inorganic carbon to produce organic matter in the dark. Their distinctive physiological traits and high abundance in the water column indicate the significant ecological roles they play in the open ocean. In our study, we found predominant Thaumarchaeota in the microbial community amended with cyanobacteria-derived lysate under the dark condition. Furthermore, Thaumarchaeota remained dominant in the microbial community even after 1 year of incubation. Through the ammonification process, dissolved organic matter (DOM) from cyanobacterial lysate was converted to ammonium which was used as an energy source for Thaumarchaeota to fix inorganic carbon into biomass. Our study further advocates the important roles of Thaumarchaeota in the ocean’s biogeochemical cycle.
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- Award ID(s):
- 1829888
- PAR ID:
- 10400403
- Editor(s):
- Weinert, Emily
- Date Published:
- Journal Name:
- Microbiology Spectrum
- Volume:
- 11
- Issue:
- 1
- ISSN:
- 2165-0497
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1128/spectrum.02405-22
