Bioenergetics evolution: the link between Earth's and Life's history

This brings us to the last point: how does bioenergetics operate? Enzymes that contain transition metals, iron–sulfur centres, flavins, hemes or other prosthetic groups catalyse the majority of bioenergetically relevant reactions (figure 2, bottom). These cofactors can simply act as electron transfer sites or have an essential role in catalysis [135]. Many of these complexes can donate (or receive) electrons directly to other proteins or, instead, transfer them to coenzymes, such as NADH or quinones. The use of cofactors in many biological processes, their universal conservation and their proven catalytic potential make them essential for any living system—without them, no organism can survive, as the investigations of autocatalytic sets in archaeal and bacterial metabolic networks clearly show [136–138]. Although with slight differences in methodology, those studies showed that the removal of cofactors and/or coenzymes from the network had a dramatic effect on the size of the recovered network. Thus, a thorough analysis regarding the possible availability of cofactors and coenzymes, also considering the evolution of their biosynthetic routes, is critical in the framework of microbial evolution. Interestingly, the first two studies identified ATP as an autocatalytic compound indispensable to kick-start metabolism, bringing us back to where this article started: microbial evolution and diversity are fuelled by the quest for ways to make ATP.

A natural link between Earth’s history and Life’s history is bioenergetics. Bioenergetics is the connection that joins two broad scientific fields: geochemistry and microbiology. To systematically elucidate the evolution and diversity of physiological traits, the functional and temporal connections between them and to create snapshots of archaeal and bacterial physiological diversity over time (figure 3), bioenergetics evolution needs to be tackled.

This endeavour requires interdisciplinary approaches that integrate phylogenies and bioinformatic screenings with, for example, biochemistry. Moreover, this could foster collaborations between bioinformaticians and experimentalists and has the potential to lead to further experimental characterizations and to produce better and more accurate predictions. Successful examples include the investigation of the evolutionary link between L-malate and L-lactate dehydrogenases, with the discovery and characterizations of a group of intermediary sequences exhibiting mixed functional properties [139], or the discovery of a new iron–sulfur centre assembly pathway coupled with the evolutionary history of the different iron–sulfur centre assembly pathways [140].

By approaching the evolution of physiology in a fundamentally modular manner, with respect to (i) proteins promoting energy-conserving redox reactions (and their different subtypes), (ii) their cofactors, (iii) their phylogenetic presence (and absence) in the temporal context of (iv) the progression of redox midpoint potentials from low (ancestral H2-dependence) to high (modern O2-dependence) during Earth history on the basis of (v) genomic and metagenomic information across modern environments, (vi) coupled with experimental characterizations of enzymes, we predict that progress can be made in understanding how extant metabolic diversity arose in a stepwise fashion, from a simpler universal ancestor.

We thank Bill Martin and Christa Schleper for their input on the initial versions of this manuscript. We also thank the Life Science Compute Cluster (LiSC) of the University of Vienna for computational support.

This work did not require ethical approval from a human subject or animal welfare committee.

A.P.: formal analysis, investigation, writing—original draft, writing—review and editing; V.K.: formal analysis, investigation, writing—original draft, writing—review and editing; J.Z.B.: formal analysis, investigation, writing—review and editing; S.N.: formal analysis, investigation, writing—original draft, writing—review and editing; F.L.S.: conceptualization, formal analysis, funding acquisition, investigation, validation, writing—original draft, writing—review and editing.

All authors gave final approval for publication and agreed to be held accountable for the work performed therein.

This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 Research and Innovation (grant agreement 803768). For funding, A.P. and S.N. acknowledge support from the Wiener Wissenschafts, Forschungs- und Technologiefonds (Austria) (grant VRG15-007 to F.L.S.), and V.K. and J.Z.B. acknowledge support from the European Research Council (ERC) under the European Union’s Horizon 2020 Research and Innovation programme (grant agreement 803768 to F.L.S.).