Primordial nitrification processes have been studied extensively using geochemical approaches, but the biological origination of nitrification remains unclear. Ammonia-oxidizing archaea (AOA) are widely distributed nitrifiers and implement the rate-limiting step in nitrification. They are hypothesized to have been important players in the global nitrogen cycle in Earth’s early history. We performed systematic phylogenomic and marker gene analyses to elucidate the diversification timeline of AOA evolution. Our results suggested that the AOA ancestor experienced terrestrial geothermal environments at ∼1,165 Ma (1,928-880 Ma), and gradually evolved into mesophilic soil at ∼652 Ma (767-554 Ma) before diversifying into marine settings at ∼509 Ma (629-412 Ma) and later into shallow and deep oceans, respectively. Corroborated by geochemical evidence and modeling, the timing of key diversification nodes can be linked to the global magmatism and glaciation associated with the assembly and breakup of the supercontinent Rodinia, and the later oxygenation of the deep ocean. Results of this integrated study shed light on the geological forces that may have shaped the evolutionary pathways of the AOA, which played an important role in the ancient global nitrogen cycle.

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Microbial community structure and metabolic activities have profound impacts on biogeochemical processes in marine sediments. Functional bacteria such as nitrate-and sulfate-reducing bacteria respond to redox gradients by coupling specific reactions amenable to relevant energy metabolisms. However, similar functional patterns have not been observed for sedimentary archaea (except for anaerobic methanotrophs and methanogens). We coupled taxonomic composition with comprehensive geochemical species to investigate the participation of distinct bacteria and archaea in sedimentary geochemical cycles in a sediment core (300 cm) from Pearl River Estuary (PRE). Geochemical properties (NO 3 − , dissolved Mn and Fe, SO 4 2+ , NH 4 + ; dissolved inorganic carbon (DIC), δ 13 C DIC , dissolved organic carbon (DOC), total organic carbon (TOC), δ 13 C TOC , and fluorescent dissolved organic matter (FDOM)) exhibited strong depth variability of different trends. Bacterial 16S rRNA-and dsrB gene abundance decreased sharply with depth while archaeal and bathyarchaeotal 16S rRNA gene copies were relatively constant. This resulted in an increase in relative abundance of archaea from surface (11.6%) to bottom (42.8%). Network analysis showed that bacterial groups of Desulfobacterales, Syntrophobacterales and Gammaproteobacteria were significantly (P < 0.0001) associated with SO 4 2− and dissolved Mn while archaeal groups of Bathyarchaeota, Group C3 and Marine Benthic Group D (MBGD) showed close positive correlations (P < 0.0001) with NH 4 + , δ 13 C TOC values and humic-like FDOM. Our study suggested that these bacterial groups dominated in redox processes relevant to sulfate or metal oxides, while the archaeal groups are more like to degrade recalcitrant organic compounds in anaerobic sediments.

Dissolved organic matter (DOM) provides carbon substrates and energy sources for sediment microbes driving benthic biogeochemical processes. The interactions between microbes and DOM are dynamic and complex and require the understanding based on fine-scale microbial community and physicochemical profiling. In this study, we characterized the porewater DOM composition in a 300-cm sediment core from the Pearl River estuary, China, and examined the interactions between DOM and archaeal and bacterial communities. DOM composition were highly stratified and associated with changing microbial communities. Compared to bacteria, the amplicon sequence variants of archaea showed significant Pearson correlations (r ≥ 0.65, P &lt; 0.01) with DOM molecules of low H/C ratios, high C number and double bond equivalents, indicating that the distribution of archaea was closely correlated to recalcitrant DOM while bacteria were associated with relatively labile compounds. This was supported by the presence of auxiliary enzyme families essential for lignin degradation and bcrABCD, UbiX genes for anaerobic aromatic reduction in metagenome-assembled genomes of Bathyarchaeia. Our study demonstrates that niche differentiation between benthic bacteria and archaea may have important consequences in carbon metabolism, particularly for the transformation of recalcitrant organic carbon that may be predominant in aged marine sediments.

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