Evolutionary History of Nickel-Dependent Enzymes : Implications for the Origins of Life.

Abstract: Nickel enzymes have been suggested, through numerous phylogenetic studies, to have been among the very first catalytic compounds on the early Earth, possibly present in the last universal common ancestor (LUCA) or prior to the onset of life. This is because of the type of reactions catalyzed by some of these enzymes, the nature of organisms that utilize them, their distribution in the tree of life, and their key roles in what is now thought of as possibly one of the oldest carbon fixation pathways, the Wood-Ljungdahl (WL) pathway. Additionally, nickel is generally thought to have been an abundant element on the early Earth, highly soluble in what were, theoretically, euxinic (anoxic and sulfidic) ocean waters. This combined with the fact that the enzymes involved in the WL pathway have an active center configuration that resembles that of minerals found in hydrothermal vent walls, makes nickel enzymes a likely candidate to have evolved from what were proto-enzymes, responsible for the prebiotic catalysis of the first simple organic molecules prior to the origins of life, according to the so-called submarine alkaline hydrothermal vent theory, first presented by Michael J. Russell in 1993 (Russell et al. 1994). In this study, I expand the known coverage on the distribution of these enzymes by mapping them in 10,575 OTUs of microbial taxa. Using their pattern of distribution, I reconstruct their histories along the branches of a reference phylogenetic tree of the same taxa through methods of ancestral reconstruction of discrete traits. Additionally, I construct an individual gene tree for each of the enzymes in order to consolidate gene history with species history. My results showed that the redox nickel enzymes (except methyl-coenzyme M reductase) are ancestral to all prokaryotes, while non-redox enzymes are derived and with multiple origins, possibly due to lateral gene transfer events or convergent evolution. I propose that the patterns observed are a product of the drastic changes during early Earth history, namely a hypothesized “nickel famine” or the Great Oxidation Event, which acted as selective pressures.