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Anaerobic thermophiles inhabit relic environments that resemble the early Earth. However, the lineage of these modern organisms co-evolved with our planet. Hence, these organisms carry both ancestral and acquired genes and serve as models to reconstruct early metabolism. Based on comparative genomic and proteomic analyses, we identified two distinct groups of genes in Thermovibrio ammonificans: the first codes for enzymes that do not require oxygen and use substrates of geothermal origin; the second appears to be a more recent acquisition, and may reflect adaptations to cope with the rise of oxygen on Earth. We propose that the ancestor of the Aquificae was originally a hydrogen oxidizing, sulfur reducing bacterium that used a hybrid pathway for CO2 fixation. With the gradual rise of oxygen in the atmosphere, more efficient terminal electron acceptors became available and this lineage acquired genes that increased its metabolic flexibility while retaining ancestral metabolic traits. DOI: http://dx.doi.org/10.7554/eLife.18990.001, eLife digest Life may have arisen on our planet as far back as four billion years ago. Unlike today, the Earth’s atmosphere at the time had no oxygen and an abundance of volcanic emissions including hydrogen, carbon dioxide and sulfur gases. These dramatic differences have led scientists to wonder: how did the ancient microorganisms that inhabited our early planet make a living? And how has microbial life co-evolved with the Earth? One way to answer these questions is to study bacteria that live today in environments that resemble the early Earth. Deep-sea hydrothermal vents are regions of the deep ocean where active volcanic processes recreate primordial conditions. These habitats support microorganisms that are highly adapted to live off hydrogen, carbon dioxide and sulfur gases, and studying these modern-day microorganisms could give insights into the earliest life on Earth. Thermovibrio ammonificans is a bacterium that was obtained from an underwater volcanic system in the East Pacific. Giovannelli et al. have now asked if T. ammonificans might have inherited some of its genetic traits from a long-gone ancestor that also thrived off volcanic gases. The genetic makeup of this microorganism was examined for genes that would help it thrive at a deep-sea hydrothermal vent. Next, Giovannelli et al. compared these genes to related copies in other species of bacteria to reconstruct how the metabolism of T. ammonificans might have changed over time. This approach identified a group of likely ancient genesthat allow a microorganism to use chemicals like hydrogen, carbon dioxide and sulfur to fuel its growth and metabolism. These findings support the hypothesis that an ancestor of T. ammonificans could live off volcanic gases and that the core set of genes involved in those activities had been passed on, through the generations, to this modern-day microorganism. Giovannelli et al. also identified a second group of genes in T. ammonificans that indicate that this bacterium also co-evolved with Earth’s changing conditions, in particular the rise in the concentration of oxygen. The findings of Giovannelli et al. provide insight into how the metabolism of microbes has co-evolved with the Earth’s changing conditions, and will allow others to formulate new hypotheses that can be tested in laboratory experiments. DOI: http://dx.doi.org/10.7554/eLife.18990.002