The Evolution Pathway of Ammonia-Oxidizing Archaea Shaped by Major Geological Events

Abstract

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.

Candidatus Nitrosopolaris, a genus of putative ammonia-oxidizing archaea with a polar/alpine distribution

“…N. rasttigaisensis, comprising MAGs obtained from mineral tundra soils in two relatively close regions in northern Fennoscandia (Kilpisjärvi and Rásttigáisá, respectively). A recent molecular dating study has suggested that the origin of the AOA clade group I.1b (order Nitrososphaerales) coincides with severe glaciation events that happened during the Neoproterozoic (Yang et al ., 2021). If these estimates are accurate, it would imply that Ca .…”

Gene inversion triggered origination of brackish archaeal heterotrophs in the aftermath of the Cryogenian Snowball Earth

“…The root of Archaea (4.38-3.46 Ga) [84][85][86] and three constraints (i.e. the roots of Thermoproteales, Sulfolobales and Thermoplasma) related to the Great Oxygenation Event (2.32 Ga) 87,88 were used for calibration as introduced in our previous study 35 .…”

“…Finally, we establish a geological time scheme in the evolution of the brackish and the marine Poseidoniales to study the possible correlation between salinity adaptation and geo-environment changes. Our recent approach has found a strong correlation between the diversification of Nitrososphaeria and geological events such as the Great Oxidation Event 35 . Building on this analytic framework, we calculated the evolutionary timepoint of Poseidoniales diversification in the phylogenetic tree of Archaea by conducting a molecular clock analysis.…”

Editorial: Ecology, Metabolism and Evolution of Archaea-Perspectives From Proceedings of the International Workshop on Geo-Omics of Archaea

“…Eukaryogenesis will continue to be a major research frontier in this area, but other important insights into archaeal evolution await. For example, recent progress on the genomic evolution of diverse archaea in the context of Earth history provide better ties between genome-based evolutionary models and the sedimentary record (e.g., Colman et al, 2018;Wang et al, 2021b;Yang et al, 2021). The fast-increasing volume and diversity of high-quality environmental genomes should lead to fruitful new ground in archaeal evolutionary studies along geological time scales, which has been hampered by the lack of physical fossils of microorganisms.…”