Interchangeable utilization of metals: New perspectives on the impacts of metal ions employed in ancient and extant biomolecules

Abstract

Metal ions provide considerable functionality across biological systems, and their utilization within biomolecules has adapted through changes in the chemical environment to maintain the activity they facilitate. While ancient earth's atmosphere was rich in iron and manganese and low in oxygen, periods of atmospheric oxygenation significantly altered the availability of certain metal ions, resulting in ion replacement within biomolecules. This adaptation mechanism has given rise to the phenomenon of metal cofactor interchangeability, whereby contemporary proteins and nucleic acids interact with multiple metal ions interchangeably, with different coordinated metals influencing biological activity, stability, and toxic potential. The ability of extant organisms to adapt to fluctuating metal availability remains relevant in a number of crucial biomolecules, including the superoxide dismutases of the antioxidant defense systems and ribonucleotide reductases. These well-studied and ancient enzymes illustrate the potential for metal interchangeability and adaptive utilization. More recently, the ribosome has also been demonstrated to exhibit interchangeable interactions with metal ions with impacts on function, stability, and stress adaptation. Using these and other examples, here we review the biological significance of interchangeable metal ions from a new angle that combines both biochemical and evolutionary viewpoints. The geochemical pressures and chemical properties that underlie biological metal utilization are discussed in the context of their impact on modern disease states and treatments.

Reconstruction of Nitrogenase Predecessors Suggests Origin from Maturase-Like Proteins

“…Identifying the singular circumstances that left Earth with a single common ancestor for all nitrogenase functions may be critical for understanding the pervasiveness of nitrogen fixation as a universal biological capability. This is particularly important for assessing whether metal availability significantly guides protein evolution or whether other internal biophysical constraints lead to background-dependent, epistatic interactions ( Williams and da Silva 1996 ; Anbar and Knoll 2002 ; Moore et al 2017 ; Smethurst and Shcherbik 2021 ). Efforts to generate artificial nitrogenases and nitrogenase metalloclusters ( Tanifuji et al 2015 ; Sickerman et al 2017 ) may expand the suite of molecular structures capable of reducing N 2 , but biotic experiments integrating gene regulatory and protein–protein interaction constraints are needed to test different macroevolutionary hypotheses of nitrogenase emergence.…”

Reconstruction of nitrogenase predecessors suggests origin from maturase-like proteins

“…Identifying the singular circumstances that left Earth with a single common ancestor for all nitrogenase function may be critical for understanding the pervasiveness of nitrogen fixation as a universal biological capability. This is particularly important for assessing whether metal availability significantly guides protein evolution or whether other internal biophysical constraints lead to background-dependent, epistatic interactions (Williams and da Silva 1996; Anbar and Knoll 2002; Moore et al 2017; Smethurst and Shcherbik 2021). Efforts to generate artificial nitrogenases and nitrogenase metalloclusters (Tanifuji et al 2015; Sickerman et al 2017) may expand the suite of molecular structures capable of reducing N 2 , but biotic experiments integrating gene regulatory and protein-protein interaction constraints are needed to test different macroevolutionary hypotheses of nitrogenase emergence.…”

Characterization of a novel superoxide dismutase in Nilaparvata lugens

“…Cells need to maintain their redox status as ROS (superoxide anion and hydrogen peroxide) tend to damage the structure and function of biomolecules such as DNA, proteins, and lipids. Antioxidant enzymes facilitate the degradation of ROS (Smethurst & Shcherbik, 2021). Major components of the antioxidant enzyme system include SOD, catalase (CAT), and glutathione S-transferase (GST).…”