A hot origin of dissimilatory sulfite reduction catalyzed by DsrAB in the Paleoarchean Era

Dissimilatory sulfite reduction (DSR) has been essential to microbial energy metabolism in the biogeochemical sulfur cycle since the Paleoarchean Era. However, due to the lack of an integrated assessment of geological record and genomic data, the evolutionary origin of DSR remains elusive in terms of time, habitat, and genetic basis. In this study, we reconstructed the evolutionary pathways and the ancestral sequences of Dsr proteins by mining metagenomes ranging from mesothermal to hyperthermal environments. A phylogenetic analysis of the key catalytic enzyme, DsrAB, and other Dsr proteins indicates that the earliest and most basic functional cascade, DsrABCNM, emerged prior to the latest common ancestor of several basal branching DsrAB clusters encoded by bacteria and archaea. Using a molecular dating strategy that calibrates the protein tree with a species tree, we predicted that the DSR originated 3.508 billion years ago (Ga). This finding strongly confirms the earliest geological evidence of DSR (~ 3.47 Ga). Further predictions from ancestral sequence reconstruction indicate that the optimal catalytic temperature of DsrA at the time of DSR origin was approximately 73°C, which is consistent with the petrographic and geochemical evidence in early Archean hydrothermal deposits. After its hot origin, DsrA diversified into subclades that adapted to various temperature levels following the Great Oxidation Event. This is exemplified by the evolution of the reductive archaeal-type DsrA. Our results synchronize the molecular ages with the geological record, which advances our understanding of the earliest DSR systems and highlights the enzymatic adaptations of microbial life in the Archean biosphere.