Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria

Matheus Carnevali, P. B.*; Schulz, F.*; Castelle, C. J.*; Kantor, R. S.*; Shih, P.*; Sharon, I.*; Santini, J.*; Olm, M. R.*; Amano, Yuki   ; Thomas, B. C.*; Anantharaman, K.*; Burstein, David*; Becraft, E. D.*; Stepanauskas, R.*; Woyke, T.*; Banfield, J. F.*

The metabolic platform in which microbial aerobic respiration evolved is tightly linked to the origins of Cyanobacteria (Oxyphotobacteria). Melainabacteria and Sericytochromatia, close phylogenetic neighbores to Oxyphotobacteria comprise both fermentative and aerobic representatives, or clades that are capablee of both. Here, we predict the metabolisms of Margulisbacteria from two distinct environments and Saganbacteria, and compare them to genomes of organisms from the related lineages. Melainabacteria BJ4A obtained from Mizunami site are potentially able to use O and other terminal electron acceptors. The type C heme-copper oxygen reductase found in Melainabacteria BJ4A may be adapted to low O levels, as expected for microaerophilic or anoxic environments such as the subsurface. Notably, Melainabacteria BJ4A seems to have a branched electron transport chain, with one branch leading to a cytochrome d ubiquinol oxidoreductase and the other one leading to the type C heme-copper oxygen reductase. Both these enzymes have high affinity for O, thus are adapted to low O levels. These contemporary lineages have representatives with fermentative H-based metabolism, lineages capable of aerobic or anaerobic respiration, and lineages with both. Our findings support the idea that the ancestor of these lineages was an anaerobe in which fermentation and H metabolism were central metabolic features.