Over the last 70 years, prebiotic chemists have been very successful in synthesizing the molecules of life, from amino acids to nucleotides. Yet there is strikingly little resemblance between much of this chemistry and the metabolic pathways of cells, in terms of substrates, catalysts, and synthetic pathways. In contrast, alkaline hydrothermal vents offer conditions similar to those harnessed by modern autotrophs, but there has been limited experimental evidence that such conditions could drive prebiotic chemistry. In the Hadean, in the absence of oxygen, alkaline vents are proposed to have acted as electrochemical flow reactors, in which alkaline fluids saturated in H₂ mixed with relatively acidic ocean waters rich in CO₂, through a labyrinth of interconnected micropores with thin inorganic walls containing catalytic Fe(Ni)S minerals. The difference in pH across these thin barriers produced natural proton gradients with equivalent magnitude and polarity to the proton-motive force required for carbon fixation in extant bacteria and archaea. How such gradients could have powered carbon reduction or energy flux before the advent of organic protocells with genes and proteins is unknown. Work over the last decade suggests several possible hypotheses that are currently being tested in laboratory experiments, field observations, and phylogenetic reconstructions of ancestral metabolism. We analyze the perplexing differences in carbon and energy metabolism in methanogenic archaea and acetogenic bacteria to propose a possible ancestral mechanism of CO₂ reduction in alkaline hydrothermal vents. Based on this mechanism, we show that the evolution of active ion pumping could have driven the deep divergence of bacteria and archaea. Key Words: Origin of life—Alkaline hydrothermal vent—Chemiosmotic coupling—Proton gradients—Methanogens—Acetogens—CO₂ reduction. Astrobiology 16, 181–197.

The nature of the last universal common ancestor (LUCA), its age and its impact on the Earth system have been the subject of vigorous debate across diverse disciplines, often based on disparate data and methods. Age estimates for LUCA are usually based on the fossil record, varying with every reinterpretation. The nature of LUCA’s metabolism has proven equally contentious, with some attributing all core metabolisms to LUCA, whereas others reconstruct a simpler life form dependent on geochemistry. Here we infer that LUCA lived ~4.2 Ga (4.09–4.33 Ga) through divergence time analysis of pre-LUCA gene duplicates, calibrated using microbial fossils and isotope records under a new cross-bracing implementation. Phylogenetic reconciliation suggests that LUCA had a genome of at least 2.5 Mb (2.49–2.99 Mb), encoding around 2,600 proteins, comparable to modern prokaryotes. Our results suggest LUCA was a prokaryote-grade anaerobic acetogen that possessed an early immune system. Although LUCA is sometimes perceived as living in isolation, we infer LUCA to have been part of an established ecological system. The metabolism of LUCA would have provided a niche for other microbial community members and hydrogen recycling by atmospheric photochemistry could have supported a modestly productive early ecosystem.

Leeuwenhoek's 1677 paper, the famous ‘letter on the protozoa’, gives the first detailed description of protists and bacteria living in a range of environments. The colloquial, diaristic style conceals the workings of a startlingly original experimental mind. Later scientists could not match the resolution and clarity of Leeuwenhoek's microscopes, so his discoveries were doubted or even dismissed over the following centuries, limiting their direct influence on the history of biology; but work in the twentieth century confirmed Leeuwenhoek's discovery of bacterial cells, with a resolution of less than 1 µm. Leeuwenhoek delighted most in the forms, interactions and behaviour of his little ‘animalcules', which inhabited a previously unimagined microcosmos. In these reflections on the scientific reach of Leeuwenhoek's ideas and observations, I equate his questions with the preoccupations of our genomic era: what is the nature of Leeuwenhoek's animalcules, where do they come from, how do they relate to each other? Even with the powerful tools of modern biology, the answers are far from resolved—these questions still challenge our understanding of microbial evolution. This commentary was written to celebrate the 350th anniversary of the journal Philosophical Transactions of the Royal Society .