Long-term partners uncoupled: Methane-munching archaea in marine sediments live closely coupled to sulfate-reducing bacteria in a syntrophic relationship. Surprisingly, however, these archaea do not necessarily need their bacterial partners to survive or grow. Scheller et al. performed stable isotope incubation experiments with deep-sea methane seep sediments (see the Perspective by Rotaru and Thamdrup). Several groups of methane-oxidizing archaea could use a range of soluble electron acceptors instead of coupling to active bacterial sulfate reduction. This decoupled pathway shows that methane-oxidizing archaea transfer electrons extracellularly and may even possess the capacity to respire iron and manganese minerals that are abundant in seafloor sediments. Science , this issue p. 703 ; see also p. 658

This paper presents a reformulation of the submarine alkaline hydrothermal theory for the emergence of life in response to recent experimental findings. The theory views life, like other self-organizing systems in the Universe, as an inevitable outcome of particular disequilibria. In this case, the disequilibria were two: (1) in redox potential, between hydrogen plus methane with the circuit-completing electron acceptors such as nitrite, nitrate, ferric iron, and carbon dioxide, and (2) in pH gradient between an acidulous external ocean and an alkaline hydrothermal fluid. Both CO ₂ and CH ₄ were equally the ultimate sources of organic carbon, and the metal sulfides and oxyhydroxides acted as protoenzymatic catalysts. The realization, now 50 years old, that membrane-spanning gradients, rather than organic intermediates, play a vital role in life's operations calls into question the idea of “prebiotic chemistry.” It informs our own suggestion that experimentation should look to the kind of nanoengines that must have been the precursors to molecular motors—such as pyrophosphate synthetase and the like driven by these gradients—that make life work. It is these putative free energy or disequilibria converters, presumably constructed from minerals comprising the earliest inorganic membranes, that, as obstacles to vectorial ionic flows, present themselves as the candidates for future experiments. Key Words: Methanotrophy—Origin of life. Astrobiology 14, 308–343.

Significance: Biology is built of organic molecules, which originate primarily from the reduction of CO ₂ through several carbon-fixation pathways. Only one of these—the Wood–Ljungdahl acetyl-CoA pathway—is energetically profitable overall and present in both Archaea and Bacteria, making it relevant to studies of the origin of life. We used geologically pertinent, life-like microfluidic pH gradients across freshly deposited Fe(Ni)S precipitates to demonstrate the first step of this pathway: the otherwise unfavorable production of formate (HCOO ^– ) from CO ₂ and H ₂ . By separating CO ₂ and H ₂ into acidic and alkaline conditions—as they would have been in early-Earth alkaline hydrothermal vents—we demonstrate a mild indirect electrochemical mechanism of pH-driven carbon fixation relevant to life’s emergence, industry, and environmental chemistry.

The evolutionary mechanisms behind the extant distribution of photosynthesis is a point of substantial contention. Hypotheses range from the presence of phototrophy in the last universal common ancestor and massive gene loss in most lineages, to a later origin in Cyanobacteria followed by extensive horizontal gene transfer into the extant phototrophic clades, with intermediate scenarios that incorporate aspects of both end-members. Here, we report draft genomes of 11 Chloroflexi: the phototrophic Chloroflexia isolate Kouleothrix aurantiaca as well as 10 genome bins recovered from metagenomic sequencing of microbial mats found in Japanese hot springs. Two of these metagenome bins encode photrophic reaction centers and several of these bins form a metabolically diverse, monophyletic clade sister to the Anaerolineae class that we term Candidatus Thermofonsia. Comparisons of organismal (based on conserved ribosomal) and phototrophy (reaction center and bacteriochlorophyll synthesis) protein phylogenies throughout the Chloroflexi demonstrate that two new lineages acquired phototrophy independently via horizontal gene transfer (HGT) from different ancestral donors within the classically phototrophic Chloroflexia class. These results illustrate a complex history of phototrophy within this group, with metabolic innovation tied to HGT. These observations do not support simple hypotheses for the evolution of photosynthesis that require massive character loss from many clades; rather, HGT appears to be the defining mechanic for the distribution of phototrophy in many of the extant clades in which it appears.