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The terrestrial subsurface microbiome contains vastly underexplored phylogenetic diversity and metabolic novelty, with critical implications for global biogeochemical cycling. Among the key microbial inhabitants of subsurface soils and sediments are Thaumarchaeota, an archaeal phylum that encompasses ammonia-oxidizing archaea (AOA) as well as non-ammonia-oxidizing basal lineages. Thaumarchaeal ecology in terrestrial systems has been extensively characterized, particularly in the case of AOA. However, there is little knowledge on the diversity and ecophysiology of Thaumarchaeota in deeper soils, as most lineages, particularly basal groups, remain uncultivated and underexplored. Here we use genome-resolved metagenomics to examine the phylogenetic and metabolic diversity of Thaumarchaeota along a 234 cm depth profile of hydrologically variable riparian floodplain sediments in the Wind River Basin near Riverton, Wyoming. Phylogenomic analysis of the metagenome-assembled genomes (MAGs) indicates a shift in AOA population structure from the dominance of the terrestrial Nitrososphaerales lineage in the well-drained top ~100 cm of the profile to the typically marine Nitrosopumilales in deeper, moister, more energy-limited sediment layers. We also describe two deeply rooting non-AOA MAGs with numerous unexpected metabolic features, including the reductive acetyl-CoA (Wood-Ljungdahl) pathway, tetrathionate respiration, a form III RuBisCO, and the potential for extracellular electron transfer. These MAGs also harbor tungsten-containing aldehyde:ferredoxin oxidoreductase, group 4f [NiFe]-hydrogenases and a canonical heme catalase, typically not found in Thaumarchaeota. Our results suggest that hydrological variables, particularly proximity to the water table, impart a strong control on the ecophysiology of Thaumarchaeota in alluvial sediments.

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. Both genomes encoded several pyrroloquinoline quinone (PQQ)-dependent alcohol dehydrogenases, as well as a form III RuBisCO. Metabolic reconstructions suggest anaplerotic CO(2) assimilation mediated by RuBisCO, which may be linked to the central carbon metabolism. 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.

Microbial activities drive the global nitrogen cycle, and in the past few years, our understanding of nitrogen cycling processes and the micro-organisms that mediate them has changed dramatically. During this time, the processes of anaerobic ammonium oxidation (anammox), and ammonia oxidation within the domain Archaea, have been recognized as two new links in the global nitrogen cycle. All available evidence indicates that these processes and organisms are critically important in the environment, and particularly in the ocean. Here we review what is currently known about the microbial ecology of anaerobic and archaeal ammonia oxidation, highlight relevant unknowns and discuss the implications of these discoveries for the global nitrogen and carbon cycles.

Nitrification plays an important role in marine biogeochemistry, yet efforts to link this process to the microorganisms that mediate it are surprisingly limited. In particular, ammonia oxidation is the first and rate-limiting step of nitrification, yet ammonia oxidation rates and the abundance of ammonia-oxidizing bacteria (AOB) have rarely been measured in tandem. Ammonia oxidation rates have not been directly quantified in conjunction with ammonia-oxidizing archaea (AOA), although mounting evidence indicates that marine Crenarchaeota are capable of ammonia oxidation, and they are among the most abundant microbial groups in the ocean. Here, we have directly quantified ammonia oxidation rates by 15N labeling, and AOA and AOB abundances by quantitative PCR analysis of ammonia monooxygenase subunit A (amoA) genes, in the Gulf of California. Based on markedly different archaeal amoA sequence types in the upper water column (60 m) and oxygen minimum zone (OMZ; 450 m), novel amoA PCR primers were designed to specifically target and quantify 'shallow' (group A) and 'deep' (group B) clades. These primers recovered extensive variability with depth. Within the OMZ, AOA were most abundant where nitrification may be coupled to denitrification. In the upper water column, group A tracked variations in nitrogen biogeochemistry with depth and between basins, whereas AOB were present in relatively low numbers or undetectable. Overall, 15NH4+ oxidation rates were remarkably well correlated with AOA group A amoA gene copies (r2=0.90, P