Phylogenomic Dating—The Relative Antiquity of Archaeal Metabolic and Physiological Traits

Abstract

Ancestral trait reconstruction was used to identify the relative ancestry of metabolic and physiological traits in the archaeal domain of life. First, well-resolved phylogenetic trees were inferred with multiple gene sequences obtained from whole genome sequences. Next, metabolic and physiological traits were coded into characters, and ancestral state reconstruction was used to identify ancient and derived traits. Traits inferred to be ancient included sulfur reduction, methanogenesis, and hydrogen oxidation. By using the articulation of the “oxygen age constraint,” several other traits were inferred to have arisen at or after 2.32 Ga: aerobic respiration, nitrate reduction, sulfate reduction, thiosulfate reduction, sulfur oxidation, and sulfide oxidation. Complex organic metabolism appeared to be nearly as ancient as autotrophy. Hyperthermophily was ancestral, while hyperacidophily and extreme halophily likely arose after 2.32 Ga. The ancestral euryarchaeote was inferred to have been a hyperthermophilic marine methanogen that lived in a deep-sea hydrothermal vent. In contrast, the ancestral crenarchaeote was most likely a hyperthermophilic sulfur reducer that lived in a slightly acidic terrestrial environment, perhaps a fumarole. Cross-colonization of these habitats may not have occurred until after 2.32 Ga, which suggests that both archaeal lineages exhibited niche specialization on early Earth for a protracted period of time. Astrobiology 9, 193–219.