Today, Mg²⁺ is an essential cofactor with diverse structural and functional roles in life's oldest macromolecular machine, the translation system. We tested whether ancient Earth conditions (low O₂, high Fe²⁺, and high Mn²⁺) can revert the ribosome to a functional ancestral state. First, SHAPE (selective 2'-hydroxyl acylation analyzed by primer extension) was used to compare the effect of Mg²⁺, Fe²⁺, and Mn²⁺ on the tertiary structure of rRNA. Then, we used in vitro translation reactions to test whether Fe²⁺ or Mn²⁺ could mediate protein production, and quantified ribosomal metal content. We found that (i) Mg²⁺, Fe²⁺, and Mn²⁺ had strikingly similar effects on rRNA folding; (ii) Fe²⁺ and Mn²⁺ can replace Mg²⁺ as the dominant divalent cation during translation of mRNA to functional protein; and (iii) Fe and Mn associate extensively with the ribosome. Given that the translation system originated and matured when Fe²⁺ and Mn²⁺ were abundant, these findings suggest that Fe²⁺ and Mn²⁺ played a role in early ribosomal evolution.