Early Microbial Evolution: The Age of Anaerobes

Abstract

In this article, the term "early microbial evolution" refers to the phase of biological history from the emergence of life to the diversification of the first microbial lineages. In the modern era (since we knew about archaea), three debates have emerged on the subject that deserve discussion: (1) thermophilic origins versus mesophilic origins, (2) autotrophic origins versus heterotrophic origins, and (3) how do eukaryotes figure into early evolution. Here, we revisit those debates from the standpoint of newer data. We also consider the perhaps more pressing issue that molecular phylogenies need to recover anaerobic lineages at the base of prokaryotic trees, because O2 is a product of biological evolution; hence, the first microbes had to be anaerobes. If molecular phylogenies do not recover anaerobes basal, something is wrong. Among the anaerobes, hydrogen-dependent autotrophs--acetogens and methanogens--look like good candidates for the ancestral state of physiology in the bacteria and archaea, respectively. New trees tend to indicate that eukaryote cytosolic ribosomes branch within their archaeal homologs, not as sisters to them and, furthermore tend to root archaea within the methanogens. These are major changes in the tree of life, and open up new avenues of thought. Geochemical methane synthesis occurs as a spontaneous, abiotic exergonic reaction at hydrothermal vents. The overall similarity between that reaction and biological methanogenesis fits well with the concept of a methanogenic root for archaea and an autotrophic origin of microbial physiology.

Figure 1.

Biological steps in the evolution of microbial metabolism as posited 45 years ago. (Based on Figure 11 in Decker et al. 1970.)

Figure 2.

A possible sequence of events in early evolution starting from alkaline hydrothermal vents. Simplified scheme of energy metabolism showing the similarities between acetate (left) and methane (right) formation from H₂ and CO₂ by acetogenic bacteria without cytochromes (the map shown is for Acetobacterium woodii, based on data in Schuchmann and Müller 2014) and hydrogenotrophic methanogenic archaea (from data in Buckel and Thauer 2013). In primitive methanogens, Na⁺ pumping is powered by the exergonic transfer of a methyl group from methanopterin to coenzyme M and the methyltransferase MtrA-H is the energy-coupling site (Buckel and Thauer 2013). In acetogens of the A. woodii type, Na⁺ pumping is powered by the exergonic transfer of electrons from ferredoxin to NAD⁺ with Rnf as energy coupling site (Schuchmann and Müller 2014). Electron bifurcation steps (Buckel and Thauer 2013) are indicated by a yellow circle—these are the reaction catalyzed by heterodisulfide reductase (archaea) and hydrogenase (bacteria). With the advent of cytochromes and quinones, respiratory chains became possible. The exploration of new environments, electron donors and terminal acceptors, expansion of available redox couples, and interdomain gene lateral gene transfers (dotted gray arrows) led to the diversification of archaeal and bacterial physiology. Metabolic end products are boxed. The acetogenic reaction is 4H₂ + 2CO₂ → CH₃COOH + 2H₂O with ΔG_o′ = –95 kJ · mol⁻¹ under standard conditions and ΔG′ = –40 kJ · mol⁻¹ at roughly physiological substrate concentrations, with an energy yield of 0.3 adenosine triphosphate (ATP) per acetate (Schuchmann and Müller 2014). The methanogenic reaction is 4H₂ + CO₂ → CH₄ + 2H₂O with ΔG_o′ = –131 kJ · mol⁻¹ under standard conditions and ΔG′ = –40 kJ · mol⁻¹ at roughly physiological substrate concentrations, with an energy yield of 0.5 ATP per methane (Buckel and Thauer 2013). Note that a hydrogenotrophic methanogen like Methanothermobacter marburgensis (Thauer et al. 2008) generates ∼40 molecules of methane for every molecule of CO₂ that is fixed as cell carbon. MFR, methanofuran; MPT tetrahydromethanopterin; CoM, coenzyme M; CoB, coenzyme B; CoM-S-S-CoB, heterodisulfide of coenzyme M and coenzyme B; Fd, ferredoxin; Eha and Ehb, energy-converting hydrogenases; MtrA-H, methyltransferase; Rnf, energy-converting ferredoxin:NADP⁺ oxidoreductase Rnf (based on data in Figure 11 in Decker et al. 1970).