title: RNA with iron(II) as a cofactor catalyses electron transfer.
abstract: Mg(2+) is essential for RNA folding and catalysis. However, for the first 1.5 billion years of life on Earth RNA inhabited an anoxic Earth with abundant and benign Fe(2+). We hypothesize that Fe(2+) was an RNA cofactor when iron was abundant, and was substantially replaced by Mg(2+) during a period known as the 'great oxidation', brought on by photosynthesis. Here, we demonstrate that reversing this putative metal substitution in an anoxic environment, by removing Mg(2+) and replacing it with Fe(2+), expands the catalytic repertoire of RNA. Fe(2+) can confer on some RNAs a previously uncharacterized ability to catalyse single-electron transfer. We propose that RNA function, in analogy with protein function, can be understood fully only in the context of association with a range of possible metals. The catalysis of electron transfer, requisite for metabolic activity, may have been attenuated in RNA by photosynthesis and the rise of O2.
authors.affiliation: School of Chemistry and Biochemistry, and NASA Astrobiology Institute Center for Ribosomal Origins and Evolution, Georgia Institute of Technology, Atlanta, Georgia 30332, USA.
authors.forename: Chiaolong
authors.initials: C
authors.lastname: Hsiao
authors.forename: I-Chun
authors.initials: IC
authors.lastname: Chou
authors.forename: C Denise
authors.initials: CD
authors.lastname: Okafor
authors.forename: Jessica C
authors.initials: JC
authors.lastname: Bowman
authors.forename: Eric B
authors.initials: EB
authors.lastname: O'Neill
authors.forename: Shreyas S
authors.initials: SS
authors.lastname: Athavale
authors.forename: Anton S
authors.initials: AS
authors.lastname: Petrov
authors.forename: Nicholas V
authors.initials: NV
authors.lastname: Hud
authors.forename: Roger M
authors.initials: RM
authors.lastname: Wartell
authors.forename: Stephen C
authors.initials: SC
authors.lastname: Harvey
authors.forename: Loren Dean
authors.initials: LD
authors.lastname: Williams
mesh_terms: D055162:Biocatalysis; D004579:Electron Transport; D007501:Iron / Q000378:metabolism*; D012313:RNA / Q000378:metabolism*
chemical_list: D012313:RNA; D007501:Iron