title: Protein domain structure uncovers the origin of aerobic metabolism and the rise of planetary oxygen.
abstract: The origin and evolution of modern biochemistry remain a mystery despite advances in evolutionary bioinformatics. Here, we use a structural census in nearly 1,000 genomes and a molecular clock of folds to define a timeline of appearance of protein families linked to single-domain enzymes. The timeline sorts out enzymatic recruitment, validates patterns in metabolic history, and reveals that the most ancient reaction of aerobic metabolism involved the synthesis of pyridoxal 5'-phosphate or pyridoxal and appeared 2.9 Gyr ago. The oxygen source for this primordial reaction was probably Mn catalase, which appeared at the same time and could have generated oxygen as a side product of hydrogen peroxide detoxification. Finally, evolutionary analysis of transferred groups and metabolite fragments revealed that oxidized sulfur did not participate in metabolism until the rise of oxygen. The evolutionary patterns we uncover in molecules and chemistries provide strong support for the coevolution of biochemistry and geochemistry.
authors.affiliation: Evolutionary Bioinformatics Laboratory, Department of Crop Sciences, University of Illinois, Urbana, IL 61801, USA.
authors.forename: Kyung Mo
authors.initials: KM
authors.lastname: Kim
authors.forename: Tao
authors.initials: T
authors.lastname: Qin
authors.forename: Ying-Ying
authors.initials: YY
authors.lastname: Jiang
authors.forename: Ling-Ling
authors.initials: LL
authors.lastname: Chen
authors.forename: Min
authors.initials: M
authors.lastname: Xiong
authors.forename: Derek
authors.initials: D
authors.lastname: Caetano-Anollés
authors.forename: Hong-Yu
authors.initials: HY
authors.lastname: Zhang
authors.forename: Gustavo
authors.initials: G
authors.lastname: Caetano-Anollés
mesh_terms: D000332:Aerobiosis; D000596:Amino Acids / Q000096:biosynthesis; D053898:Biosynthetic Pathways / Q000235:genetics*; D002374:Catalase / Q000378:metabolism; D019143:Evolution, Molecular; D023281:Genomics / Q000379:methods; D008958:Models, Molecular; D015394:Molecular Structure; D010100:Oxygen / Q000737:chemistry / Q000378:metabolism*; D010802:Phylogeny; D017510:Protein Folding; D017434:Protein Structure, Tertiary; D011506:Proteins / Q000737:chemistry*; D011732:Pyridoxal Phosphate / Q000096:biosynthesis / Q000378:metabolism
chemical_list: D000596:Amino Acids; D011506:Proteins; D011732:Pyridoxal Phosphate; D002374:Catalase; D010100:Oxygen