Aerobic heterotrophy and RuBisCO-mediated CO2 metabolism in marine Thaumarchaeota

Thaumarchaeota constitute an abundant and ubiquitous phylum of Archaea that play critical roles in the global nitrogen and carbon cycles. Most well-characterized members of the phylum are chemolithoautotrophic ammonia-oxidizing archaea (AOA), which comprise up to 5 and 20 % of the total single-celled life in soil and marine systems, respectively. Using two high-quality metagenome-assembled genomes (MAGs), here we describe a divergent marine thaumarchaeal clade that is devoid of the ammonia-oxidation machinery and the AOA-specific carbon-fixation pathway. Phylogenomic analyses placed these genomes within the uncultivated and largely understudied marine pSL12-like thaumarchaeal clade. The predominant mode of nutrient acquisition appears to be aerobic heterotrophy, evidenced by the presence of respiratory complexes and various organic carbon degradation pathways. Unexpectedly, both genomes encoded a form III RuBisCO. Genomic composition of the MAGs is consistent with the role of RuBisCO in nucleotide salvage, as has been proposed previously for archaea harboring the form III variant. Metabolic reconstructions revealed a complete nonoxidative pentose phosphate pathway (PPP) and gluconeogenesis, which can cyclize the RuBisCO-mediated carbon metabolic pathway. We conclude that these genomes represent a hitherto unrecognized evolutionary link between predominantly anaerobic basal thaumarchaeal lineages and mesophilic marine AOA, with important implications for diversification within the phylum Thaumarchaeota.