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Methanogenic archaea are major producers of methane, a potent greenhouse gas and biofuel, and are widespread in diverse environments, including the animal gut. The ecophysiology of methanogens is likely impacted by viruses, which remain, however, largely uncharacterized. Here we carried out a global investigation of viruses associated with all current diversity of methanogens by assembling an extensive CRISPR database consisting of 156,000 spacers. We report 282 high-quality (pro)viral and 205 virus-like/plasmid sequences assigned to hosts belonging to ten main orders of methanogenic archaea. Viruses of methanogens can be classified into 87 families, underscoring a still largely undiscovered genetic diversity. Viruses infecting gut-associated archaea provide evidence of convergence in adaptation with viruses infecting gut-associated bacteria. These viruses contain a large repertoire of lysin proteins that cleave archaeal pseudomurein and are enriched in glycan-binding domains (Ig-like/Flg_new) and diversity-generating retroelements. The characterization of this vast repertoire of viruses paves the way towards a better understanding of their role in regulating methanogen communities globally, as well as the development of much-needed genetic tools., (© 2023. The Author(s), under exclusive licence to Springer Nature Limited.)

DNA in cells is associated with proteins that constrain its structure and affect DNA-templated processes including transcription and replication. HU and histones are the main constituents of chromatin in bacteria and eukaryotes, respectively, with few exceptions. Archaea, in contrast, have diverse repertoires of nucleoid-associated proteins (NAPs). To analyse the evolutionary and ecological drivers of this diversity, we combined a phylogenomic survey of known and predicted NAPs with quantitative proteomic data. We identify the Diaforarchaea as a hotbed of NAP gain and loss, and experimentally validate candidate NAPs in two members of this clade, Thermoplasma volcanium and Methanomassiliicoccus luminyensis. Proteomic analysis across a diverse sample of 19 archaea revealed that NAP investment varies from <0.03% to >5% of total protein. This variation is predicted by growth temperature. We propose that high levels of chromatinization have evolved as a mechanism to prevent uncontrolled helix denaturation at higher temperatures, with implications for the origin of chromatin in both archaea and eukaryotes., (© 2022. The Author(s).)

The human gut microbiome plays an important role in health, but its archaeal diversity remains largely unexplored. In the present study, we report the analysis of 1,167 nonredundant archaeal genomes (608 high-quality genomes) recovered from human gastrointestinal tract, sampled across 24 countries and rural and urban populations. We identified previously undescribed taxa including 3 genera, 15 species and 52 strains. Based on distinct genomic features, we justify the split of the Methanobrevibacter smithii clade into two separate species, with one represented by the previously undescribed 'Candidatus Methanobrevibacter intestini'. Patterns derived from 28,581 protein clusters showed significant associations with sociodemographic characteristics such as age groups and lifestyle. We additionally show that archaea are characterized by specific genomic and functional adaptations to the host and carry a complex virome. Our work expands our current understanding of the human archaeome and provides a large genome catalogue for future analyses to decipher its impact on human physiology., (© 2021. The Author(s).)

The tetrahydromethanopterin (H 4 MPT) methyl branch of the Wood-Ljungdahl pathway is shared by archaeal and bacterial metabolisms that greatly contribute to the global carbon budget and greenhouse gas fluxes: methanogenesis and methylotrophy, including methanotrophy 1-3 . It has been proposed that the H 4 MPT branch dates back to the last universal common ancestor 4-6 . Interestingly, it has been identified in numerous recently sequenced and mostly uncultured non-methanogenic and non-methylotrophic archaeal and bacterial lineages, where its function remains unclear 5,7 . Here, we have examined the distribution and phylogeny of the enzymes involved in the H 4 MPT branch and the biosynthesis of its cofactors in over 6,400 archaeal and bacterial genomes. We find that a full Wood-Ljungdahl H 4 MPT pathway is widespread in Archaea and is likely ancestral to this domain, whereas this is not the case for Bacteria. Moreover, the inclusion of recently sequenced lineages leads to an important shortening of the branch separating Archaea and Bacteria with respect to previous phylogenies of the H 4 MPT branch. Finally, the genes for the pathway are colocalized in many of the recently sequenced archaeal lineages, similar to bacteria. Together, these results weaken the last universal common ancestor hypothesis and rather favour an origin of the H 4 MPT branch in Archaea and its subsequent transfer to Bacteria. We propose a scenario for its potential initial role in the first bacterial recipients and its evolution up to the emergence of aerobic methylotrophy. Finally, we discuss how an ancient horizontal transfer not only triggered the emergence of key metabolic processes but also important transitions in Earth's history.

Methanogenesis is an ancient metabolism of key ecological relevance, with direct impact on the evolution of Earth's climate. Recent results suggest that the diversity of methane metabolisms and their derivations have probably been vastly underestimated. Here, by probing thousands of publicly available metagenomes for homologues of methyl-coenzyme M reductase complex (MCR), we have obtained ten metagenome-assembled genomes (MAGs) belonging to potential methanogenic, anaerobic methanotrophic and short-chain alkane-oxidizing archaea. Five of these MAGs represent under-sampled (Verstraetearchaeota, Methanonatronarchaeia, ANME-1 and GoM-Arc1) or previously genomically undescribed (ANME-2c) archaeal lineages. The remaining five MAGs correspond to lineages that are only distantly related to previously known methanogens and span the entire archaeal phylogeny. Comprehensive comparative annotation substantially expands the metabolic diversity and energy conservation systems of MCR-bearing archaea. It also suggests the potential existence of a yet uncharacterized type of methanogenesis linked to short-chain alkane/fatty acid oxidation in a previously undescribed class of archaea ('Candidatus Methanoliparia'). We redefine a common core of marker genes specific to methanogenic, anaerobic methanotrophic and short-chain alkane-oxidizing archaea, and propose a possible scenario for the evolutionary and functional transitions that led to the emergence of such metabolic diversity.