Methanogenesis and anaerobic methane oxidation through methyl-coenzyme M reductase (MCR) as a key enzyme have been suggested to be basal pathways of archaea 1 . How widespread MCR-based alkane metabolism is among archaea, where it occurs and how it evolved remain elusive. Here, we performed a global survey of MCR-encoding genomes based on metagenomic data from various environments. Eleven high-quality mcr-containing metagenomic-assembled genomes were obtained belonging to the Archaeoglobi in the Euryarchaeota, Hadesarchaeota and different TACK superphylum archaea, including the Nezhaarchaeota, Korarchaeota and Verstraetearchaeota. Archaeoglobi WYZ-LMO1 and WYZ-LMO3 and Korarchaeota WYZ-LMO9 encode both the (reverse) methanogenesis and the dissimilatory sulfate reduction pathway, suggesting that they have the genomic potential to couple both pathways in individual organisms. The Hadesarchaeota WYZ-LMO4-6 and Archaeoglobi JdFR-42 encode highly divergent MCRs, enzymes that may enable them to thrive on non-methane alkanes. The occurrence of mcr genes in different archaeal phyla indicates that MCR-based alkane metabolism is common in the domain of Archaea.Since the emergence of life on our planet, anaerobic methane metabolism, including methanogenesis and methane oxidation, has been a crucial element in the Earth's carbon cycle 1 , and both processes are key to the global methane budget. Methanogenic archaea produce ~500-600 Tg of methane per year 2 , whereas anaerobic methane-oxidizing archaea (ANME) oxidize a large portion of methane within the seafloor before it reaches the water column 3,4 . The metabolic pathways of methane formation and anaerobic oxidation of methane are largely identical, as both contain exclusively C 1 -compound-transforming enzymes that were described originally in the methanogenesis pathway [5][6][7] .Among these enzymes, methyl-coenzyme M (CoM) reductase (MCR) plays the crucial role 8 . In methanogens, MCR reduces CH 3 -CoM to CH 4 (refs. 9,10 ), whereas in ANMEs, this enzyme activates CH 4 to form CH 3 -CoM as the primary intermediate 5 . This canonical MCR type is highly conserved, and the gene encoding the α-subunit (mcrA) of the enzyme complex has been used as a diagnostic marker for the detection and phylogenetic classification of methanogens and ANMEs 11 . The presence of MCR was thought to be limited to the phylum Euryarchaeota, yet the occurrence of mcr genes in metagenome-assembled genomes (MAGs) of the Bathyarchaeota 12 and Verstraetearchaeota 13 has indicated a much wider distribution of this gene within archaea. In addition, highly divergent MCR types have been identified in two strains of the thermophilic Ca. Syntrophoarchaeum spp. that use the encoded enzymes to activate

Microbes that synthesize minerals, a process known as microbial biomineralization, contributed substantially to the evolution of current planetary environments through numerous important geochemical processes. Despite its geological significance, the origin and evolution of microbial biomineralization remain poorly understood. Through combined metagenomic and phylogenetic analyses of deep-branching magnetotactic bacteria from the Nitrospirae phylum, and using a Bayesian molecular clock-dating method, we show here that the gene cluster responsible for biomineralization of magnetosomes, and the arrangement of magnetosome chain(s) within cells, both originated before or near the Archean divergence between the Nitrospirae and Proteobacteria. This phylogenetic divergence occurred well before the Great Oxygenation Event. Magnetotaxis likely evolved due to environmental pressures conferring an evolutionary advantage to navigation via the geomagnetic field. Earth's dynamo must therefore have been sufficiently strong to sustain microbial magnetotaxis in the Archean, suggesting that magnetotaxis coevolved with the geodynamo over geological time.Archean | microbial biomineralization | magnetotaxis | magnetotactic bacteria | geodynamo

As the most abundant biological entities on the planet, viruses significantly influence the overall functioning of marine ecosystems. The abundance, distribution, and biodiversity of viral communities in the upper ocean have been relatively well studied, but our understanding of viruses in the hadal biosphere remains poor. Here, we established the oceanic trench viral genome dataset (OTVGD) by analysing 19 microbial metagenomes derived from seawater and sediment samples of the Mariana, Yap, and Kermadec Trenches. The trench viral communities harbored remarkably high novelty, and they were predicted to infect ecologically important microbial clades, including Thaumarchaeota and Oleibacter. Significant inter-trench and intra-trench exchange of viral communities was proposed. Moreover, viral communities in different habitats (seawater/sediment and depth-stratified ocean zones) exhibited distinct niche-dependent distribution patterns and genomic properties. Notably, microbes and viruses in the hadopelagic seawater seemed to preferably adopt lysogenic lifestyles compared to those in the upper ocean. Furthermore, niche-specific auxiliary metabolic genes were identified in the hadal viral genomes, and a novel viral D-amino acid oxidase was functionally and phylogenetically characterized, suggesting the contribution of these genes in the utilization of refractory organic matter. Together, these findings highlight the genomic novelty, dynamic movement, and environment-driven diversification of viral communities in oceanic trenches, and suggest that viruses may influence the hadal ecosystem by reprogramming the metabolism of their hosts and modulating the community of keystone microbes.