Proceedings of the National Academy of Sciences

Methanogenic archaea are major contributors to the global carbon cycle and were long thought to belong exclusively to the euryarchaeal phylum. Discovery of the methanogenesis gene cluster methyl-coenzyme M reductase (Mcr) in the Bathyarchaeota, and thereafter the Verstraetearchaeota, led to a paradigm shift, pushing back the evolutionary origin of methanogenesis to predate that of the Euryarchaeota. The methylotrophic methanogenesis found in the non-Euryarchaota distinguished itself from the predominantly hydrogenotrophic methanogens found in euryarchaeal orders as the former do not couple methanogenesis to carbon fixation through the reductive acetyl-CoA [Wood–Ljungdahl pathway (WLP)], which was interpreted as evidence for independent evolution of the two methanogenesis pathways. Here, we report the discovery of a complete and divergent hydrogenotrophic methanogenesis pathway in a thermophilic order of the Verstraetearchaeota, which we have named Candidatus Methanohydrogenales, as well as the presence of the WLP in the crenarchaeal order Desulfurococcales. Our findings support the ancient origin of hydrogenotrophic methanogenesis, suggest that methylotrophic methanogenesis might be a later adaptation of specific orders, and provide insight into how the transition from hydrogenotrophic to methylotrophic methanogenesis might have occurred.

Significance Phosphite (HPO 3 2− ) is the most energetically favorable biological electron donor known, but only one organism capable of growing by phosphite oxidation has been previously identified. Here, we describe a phosphite-oxidizing bacterium that can grow with CO 2 as its sole electron acceptor, and we propose a metabolic model in which inorganic carbon is assimilated via the reductive glycine pathway. Although the reductive glycine pathway has previously been identified as a “synthetic” carbon fixation pathway, this study provides evidence that it may actually function as a natural autotrophic pathway. Our results suggest that phosphite may serve as a driver of microbial growth and carbon fixation in energy-limited environments, particularly in aphotic environments lacking alternative terminal electron acceptors.

Significance Gastrointestinal symbionts of organisms are important in the breakdown of food for the host, particularly for herbivores requiring exogenous enzymes to digest complex polysaccharides in their diet. However, their role in the digestion of algae in marine piscine herbivores remains unresolved. Here, we show that the diversity of food sources available to herbivorous surgeonfishes is directly linked with the genetic makeup of their enteric microbiota. Importantly, the genomic blueprint of dominant enteric symbionts belonging to diverse Epulopiscium clades differs according to the host diet. Thus, the acquisition of a unique enteric microbiota specialized to their diets likely shapes the nutritional ecology of piscine herbivores, in turn facilitating the coexistence of a high diversity of marine species within coral reefs.

Significance The Deepwater Horizon drilling accident was the first major release of oil and natural gases in the deep ocean, and considerable uncertainty remains about the fate of vast amounts of hydrocarbons that never reached the surface. We simulated the deep-sea plumes of dispersed oil microdroplets and measured biodegradation of crude oil components. We successfully reproduced the successive blooms of diverse bacteria observed in the field and obtained near-complete genomes of all major hydrocarbon-degrading species, providing an assessment of the metabolic capabilities of the microbial community responsible for biodegradation. Our results show that rapidly degraded components of oil were consumed by bacteria with highly specialized degradation capabilities and that crude oil alone could explain the microbial dynamics observed in the field.

Significance A wide range of organisms sense Earth’s magnetic field for navigation. For some organisms, like magnetotactic bacteria, magnetic particles form inside cells and act like a compass. However, the origin of magnetotactic behavior remains a mystery. We report that magnetotaxis evolved in bacteria during the Archean, before or near the divergence between the Nitrospirae and Proteobacteria phyla, suggesting that magnetotactic bacteria are one of the earliest magnetic-sensing and biomineralizing organisms on Earth. The early origin for magnetotaxis would have provided evolutionary advantages in coping with environmental challenges faced by microorganisms on early Earth. The persistence of magnetotaxis in separate lineages implies the temporal continuity of geomagnetic field, and this biological evidence provides a constraint on the evolution of the geodynamo.

Significance Mealybugs are plant sap-sucking insects with a nested symbiotic arrangement, where one bacterium lives inside another bacterium, which together live inside insect cells. These two bacteria, along with genes transferred from other bacteria to the insect genome, allow the insect to survive on its nutrient-poor diet. Here, we show that the innermost bacterium in this nested symbiosis was replaced several times over evolutionary history. These results show that highly integrated and interdependent symbiotic systems can experience symbiont replacement and suggest that similar dynamics could have occurred in building the mosaic metabolic pathways seen in mitochondria and plastids.

Significance Thaumarchaeota are among the most abundant microbial cells in the ocean, but to date, complete genome sequences for marine Thaumarchaeota are lacking. Here, we report the 1.23-Mbp genome of the pelagic ammonia-oxidizing thaumarchaeon “ Candidatus Nitrosopelagicus brevis” str. CN25. We present the first proteomic data, to our knowledge, from this phylum, which show a high proportion of proteins translated in oligotrophic conditions. Metagenomic fragment recruitment using data from the open ocean indicate the ubiquitous presence of Ca. N. brevis-like sequences in the surface ocean and suggest Ca . N. brevis as a model system for understanding the ecology and evolution of pelagic marine Thaumarchaeota.

Significance TM7 is one of the most enigmatic bacterial phyla among the uncultivated candidate phyla referred to as “microbial dark matter,” and it has potential pathogenic associations. We revealed molecular insights into its uncultivability and pathogenicity, as well its unique epibiotic and parasitic lifestyle phases. These novel discoveries shed significant light on the biological, ecological, and medical importance of TM7, as well as providing useful information for culturing other TM7 and currently uncultivable bacteria that may evade standard cultivation approaches.

Secondary metabolites are ubiquitous in bacteria, but by definition, they are thought to be nonessential. Highly toxic secondary metabolites such as patellazoles have been isolated from marine tunicates, where their exceptional potency and abundance implies a role in chemical defense, but their biological source is unknown. Here, we describe the association of the tunicate Lissoclinum patella with a symbiotic α-proteobacterium, Candidatus Endolissoclinum faulkneri, and present chemical and biological evidence that the bacterium synthesizes patellazoles. We sequenced and assembled the complete Ca . E. faulkneri genome, directly from metagenomic DNA obtained from the tunicate, where it accounted for 0.6% of sequence data. We show that the large patellazoles biosynthetic pathway is maintained, whereas the remainder of the genome is undergoing extensive streamlining to eliminate unneeded genes. The preservation of this pathway in streamlined bacteria demonstrates that secondary metabolism is an essential component of the symbiotic interaction.

Nitrification is a fundamental component of the global nitrogen cycle and leads to significant fertilizer loss and atmospheric and groundwater pollution. Nitrification rates in acidic soils (pH < 5.5), which comprise 30% of the world's soils, equal or exceed those of neutral soils. Paradoxically, autotrophic ammonia oxidizing bacteria and archaea, which perform the first stage in nitrification, demonstrate little or no growth in suspended liquid culture below pH 6.5, at which ammonia availability is reduced by ionization. Here we report the discovery and cultivation of a chemolithotrophic, obligately acidophilic thaumarchaeal ammonia oxidizer, “ Candidatus Nitrosotalea devanaterra,” from an acidic agricultural soil. Phylogenetic analysis places the organism within a previously uncultivated thaumarchaeal lineage that has been observed in acidic soils. Growth of the organism is optimal in the pH range 4 to 5 and is restricted to the pH range 4 to 5.5, unlike all previously cultivated ammonia oxidizers. Growth of this organism and associated ammonia oxidation and autotrophy also occur during nitrification in soil at pH 4.5. The discovery of Nitrosotalea devanaterra provides a previously unsuspected explanation for high rates of nitrification in acidic soils, and confirms the vital role that thaumarchaea play in terrestrial nitrogen cycling. Growth at extremely low ammonia concentration (0.18 nM) also challenges accepted views on ammonia uptake and metabolism and indicates novel mechanisms for ammonia oxidation at low pH.