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.

Ancestral Reconstructions Decipher Major Adaptations of Ammonia-Oxidizing Archaea upon Radiation into Moderate Terrestrial and Marine Environments

“…The inference of an aerobic ancestor stands in contrast to a recent study (27) that concluded LACAOA arose from an anaerobic ancestor, based on the assumption that all lineages basal to AOA are anaerobic (i.e., non-AOA Thaumarchaeota, Aigarchaeota and Bathyarchaeota). However, most Aigarchaeota and at least two non-AOA Thaumarchaeota (BS4 and pSL12) included in our data set were predicted to be facultative aerobes-the latter being recently further supported by a study reporting metagenome-assembled genomes from the pSL12 lineage with potential for aerobic respiration (22,(41)(42)(43)(44). In our ancestral reconstructions, genes involved in anaerobic metabolisms were inferred as gains in the respective lineages, such as the codH subunits in the ancestor of Bathyarchaeota or nitrate reductase and adenylylsulfate reductase families in Thaumarchaeota BS4 and DS1.…”

Time-series transcriptomics from cold, oxic subseafloor crustal fluids reveals a motile, mixotrophic microbial community

“…We did not detect the 4-hydroxybutyrate/ 3-hydroxypropionate cycle used by ammonia-oxidizing archaea for carbon fixation [78] in any of our samples. However, culturing, DNA stable isotope probing, and MAG data suggest many of these archaea may be mixotrophic or heterotrophic [79][80][81][82][83].…”

Community, Distribution, and Ecological Roles of Estuarine Archaea

“…Previous studies suggested that some members of Thaumarchaeota are non-AOA and are discovered in diverse environments ( Rinke et al, 2013 ; Weber et al, 2015 ; Hua et al, 2018 ; Aylward and Santoro, 2020 ). Members of non-AOA represent the deepest lineages in the phylogenetic tree of Thaumarchaeota , forming the basal group (Group I.1c) ( Beam et al, 2014 ; Hua et al, 2018 ).…”

“…Intriguingly, a group of heterotopic marine Thaumarchaeota , a sister group close to AOA rather than affiliated to the basal group, lacks the ability to oxidize ammonia and to engage in AOA-specific carbon-fixation ( Aylward and Santoro, 2020 ; Reji and Francis, 2020 ). Based on metagenomics data, this group is widespread in marine environments, has smaller genome sizes than AOA, and encode the form III ribulose-bisphosphate carboxylase (RuBisCO) that potentially functions in nucleotide scavenging ( Aylward and Santoro, 2020 ; Reji and Francis, 2020 ). The discovery of this group altered the knowledge of the metabolic diversity of Thaumarchaeota , and established solid connection between the basal non-AOA and AOA groups.…”