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The Genome Taxonomy Database is a phylogenetically consistent, genome-based taxonomy that provides rank-normalized classifications for ~150,000 bacterial and archaeal genomes from domain to genus. However, almost 40% of the genomes in the Genome Taxonomy Database lack a species name. We address this limitation by using commonly accepted average nucleotide identity criteria to set bounds on species and propose species clusters that encompass all publicly available bacterial and archaeal genomes. Unlike previous average nucleotide identity studies, we chose a single representative genome to serve as the effective nomenclatural ‘type’ defining each species. Of the 24,706 proposed species clusters, 8,792 are based on published names. We assigned placeholder names to the remaining 15,914 species clusters to provide names to the growing number of genomes from uncultivated species. This resource provides a complete domain-to-species taxonomic framework for bacterial and archaeal genomes, which will facilitate research on uncultivated species and improve communication of scientific results.A full species classification is built for all publicly available bacterial and archaeal genomes.

Interpretation of microbial genome data will be improved by a fully revised bacterial taxonomy. Taxonomy is an organizing principle of biology and is ideally based on evolutionary relationships among organisms. Development of a robust bacterial taxonomy has been hindered by an inability to obtain most bacteria in pure culture and, to a lesser extent, by the historical use of phenotypes to guide classification. Culture-independent sequencing technologies have matured sufficiently that a comprehensive genome-based taxonomy is now possible. We used a concatenated protein phylogeny as the basis for a bacterial taxonomy that conservatively removes polyphyletic groups and normalizes taxonomic ranks on the basis of relative evolutionary divergence. Under this approach, 58% of the 94,759 genomes comprising the Genome Taxonomy Database had changes to their existing taxonomy. This result includes the description of 99 phyla, including six major monophyletic units from the subdivision of the Proteobacteria, and amalgamation of the Candidate Phyla Radiation into a single phylum. Our taxonomy should enable improved classification of uncultured bacteria and provide a sound basis for ecological and evolutionary studies.

The classification of life forms into a hierarchical system (taxonomy) and the application of names to this hierarchy (nomenclature) is at a turning point in microbiology. The unprecedented availability of genome sequences means that a taxonomy can be built upon a comprehensive evolutionary framework, a longstanding goal of taxonomists. However, there is resistance to adopting a single framework to preserve taxonomic freedom, and ever increasing numbers of genomes derived from uncultured prokaryotes threaten to overwhelm current nomenclatural practices, which are based on characterised isolates. The challenge ahead then is to reach a consensus on the taxonomic framework and to adapt and scale the existing nomenclatural code, or create a new code, to systematically incorporate uncultured taxa into the chosen framework.

Challenges in cultivating microorganisms have limited the phylogenetic diversity of currently available microbial genomes. This is being addressed by advances in sequencing throughput and computational techniques that allow for the cultivation-independent recovery of genomes from metagenomes. Here, we report the reconstruction of 7,903 bacterial and archaeal genomes from >1,500 public metagenomes. All genomes are estimated to be ≥50% complete and nearly half are ≥90% complete with ≤5% contamination. These genomes increase the phylogenetic diversity of bacterial and archaeal genome trees by >30% and provide the first representatives of 17 bacterial and three archaeal candidate phyla. We also recovered 245 genomes from the Patescibacteria superphylum (also known as the Candidate Phyla Radiation) and find that the relative diversity of this group varies substantially with different protein marker sets. The scale and quality of this data set demonstrate that recovering genomes from metagenomes provides an expedient path forward to exploring microbial dark matter. The recovery of 7,903 bacterial and archaeal metagenome-assembled genomes increases the phylogenetic diversity represented by public genome repositories and provides the first representatives from 20 candidate phyla.

Marine Group II (MGII) archaea represent the most abundant planktonic archaeal group in ocean surface waters, but our understanding of the group has been limited by a lack of cultured representatives and few sequenced genomes. Here, we conducted a comparative phylogenomic analysis of 270 recently available MGII metagenome-assembled genomes (MAGs) to investigate their evolution and ecology. Based on a rank-normalised genome phylogeny, we propose that MGII is an order-level lineage for which we propose the name Candidatus Poseidoniale s (after Gr. n. Poseidon, God of the sea), comprising the families Candidatus Poseidonaceae fam. nov. (formerly subgroup MGIIa) and Candidatus Thalassarchaeaceae fam. nov. (formerly subgroup MGIIb). Within these families, 21 genera could be resolved, many of which had distinct biogeographic ranges and inferred nutrient preferences. Phylogenetic analyses of key metabolic functions suggest that the ancestor of Ca . Poseidoniales was a surface water-dwelling photoheterotroph that evolved to occupy multiple related ecological niches based primarily on spectral tuning of proteorhodopsin genes. Interestingly, this adaptation appears to involve an overwrite mechanism whereby an existing single copy of the proteorhodopsin gene is replaced by a horizontally transferred copy, which in many instances should allow an abrupt change in light absorption capacity. Phototrophy was lost entirely from five Ca . Poseidoniales genera coinciding with their adaptation to deeper aphotic waters. We also report the first instances of nitrate reductase in two genera acquired via horizontal gene transfer (HGT), which was a potential adaptation to oxygen limitation. Additional metabolic traits differentiating families and genera include flagellar-based adhesion, transporters, and sugar, amino acid, and peptide degradation. Our results suggest that HGT has shaped the evolution of Ca . Poseidoniales to occupy a variety of ecological niches and to become the most successful archaeal lineage in ocean surface waters.

The accrual of genomic data from both cultured and uncultured microorganisms provides new opportunities to develop systematic taxonomies based on evolutionary relationships. Previously, we established a bacterial taxonomy through the Genome Taxonomy Database. Here, we propose a standardized archaeal taxonomy that is derived from a 122-concatenated-protein phylogeny that resolves polyphyletic groups and normalizes ranks based on relative evolutionary divergence. The resulting archaeal taxonomy, which forms part of the Genome Taxonomy Database, is stable for a range of phylogenetic variables including marker gene selection, inference methods, corrections for rate heterogeneity and compositional bias, tree rooting scenarios and expansion of the genome database. Rank normalization is shown to robustly correct for substitution rates varying up to 30-fold using simulated datasets. Taxonomic curation follows the rules of the International Code of Nomenclature of Prokaryotes while taking into account proposals to formally recognize the rank of phylum and to use genome sequences as type material. This taxonomy is based on 2,392 archaeal genomes, 93.3% of which required one or more changes to their existing taxonomy, mainly owing to incomplete classification. We identify 16 archaeal phyla and reclassify 3 major monophyletic units from the former Euryarchaeota and one phylum that unites the Thaumarchaeota–Aigarchaeota–Crenarchaeota–Korarchaeota (TACK) superphylum into a single phylum. Resolving widespread incomplete and uneven archaeal classifications is achieved by a rank-normalized genome-based taxonomy.

The lack of microbial genomes and isolates from the deep seabed means that very little is known about the ecology of this vast habitat. Here, we investigate energy and carbon acquisition strategies of microbial communities from three deep seabed petroleum seeps (3 km water depth) in the Eastern Gulf of Mexico. Shotgun metagenomic analysis reveals that each sediment harbors diverse communities of chemoheterotrophs and chemolithotrophs. We recovered 82 metagenome-assembled genomes affiliated with 21 different archaeal and bacterial phyla. Multiple genomes encode enzymes for anaerobic oxidation of aliphatic and aromatic compounds, including those of candidate phyla Aerophobetes, Aminicenantes, TA06 and Bathyarchaeota. Microbial interactions are predicted to be driven by acetate and molecular hydrogen. These findings are supported by sediment geochemistry, metabolomics, and thermodynamic modelling. Overall, we infer that deep-sea sediments experiencing thermogenic hydrocarbon inputs harbor phylogenetically and functionally diverse communities potentially sustained through anaerobic hydrocarbon, acetate and hydrogen metabolism. Little is known about the microbial ecology of the deep seabed. Here, Dong et al. predict metabolic capabilities and microbial interactions in deep seabed petroleum seeps using shotgun metagenomics, sediment geochemistry, metabolomics, and thermodynamic modelling.

Most prokaryotes are not available as pure cultures and therefore ineligible for naming under the rules and recommendations of the International Code of Nomenclature of Prokaryotes (ICNP). Here we summarize the development of the SeqCode, a code of nomenclature under which genome sequences serve as nomenclatural types. This code enables valid publication of names of prokaryotes based upon isolate genome, metagenome-assembled genome or single-amplified genome sequences. Otherwise, it is similar to the ICNP with regard to the formation of names and rules of priority. It operates through the SeqCode Registry (https://seqco.de/), a registration portal through which names and nomenclatural types are registered, validated and linked to metadata. We describe the two paths currently available within SeqCode to register and validate names, including Candidatus names, and provide examples for both. Recommendations on minimal standards for DNA sequences are provided. Thus, the SeqCode provides a reproducible and objective framework for the nomenclature of all prokaryotes regardless of cultivability and facilitates communication across microbiological disciplines.

Antarctic lake ecosystems provide a rare opportunity to study the evolution and adaptation of microorganisms to extreme conditions, as well as to discover new species useful for biotechnological applications. Four water samples were collected from various layers of the water column of freshwater Lake Radok in East Antarctica. Two regions (v3-v5 and v4-v8) of the 16S rRNA gene were amplified by PCR and sequenced. Twenty dominant phylotypes were detected representing five bacterial phyla (Actinobacteria, α, β and δ Proteobacteria, Bacteroidetes, Planctomycetes, OD1) and two eukaryotic divisions (stramenopiles and green algae). Of these, 16 phylotypes demonstrated ≤98 % identity to the nearest taxa in GenBank and were therefore classified as new unknown species. Seven phylotypes demonstrated ≤90 % identity and thus remained unidentified. Actinobacteria was the most abundant phylum with 157 clones (41 % of the total number) representing 5 phylotypes. A species complex (3 clades from acI-A subgroup) of Candidatus Planktophila limnetica was prevalent in all layers. Representatives of the OD1 phylum and δ-proteobacteria were discovered by sequencing of the v3-v5 region of 16S rRNA, while Planctomycetes, β-proteobacteria and mtDNA of stramenopiles were discovered by sequencing of the v4-v8 region. This highlights the necessity of sequencing at least two 16S rRNA gene regions to gain more data on microbial community characterization. In general, despite the uniformity in the physical and chemical properties in the water column, a prominent stratification of microbial groups was observed, at the levels of both divisions and phylotypes.

The significance of this research extends to understanding microbial survival and adaptation in oligotrophic environments, such as those found in SAF. Whole-genome sequencing of several strains isolated from Mars 2020 mission assembly cleanroom facilities, including the discovery of the novel species Tigheibacillus jepli , highlights the resilience and antimicrobial resistance (AMR) in clinically relevant antibiotic classes of microbes in nutrient-scarce settings. The study also redefines the taxonomic classifications within the Amphibacillaceae family, aligning genetic identities with phylogenetic data. Investigating ARG and virulence factors (VF) across these strains illuminates the microbial capability for resistance under resource-limited conditions while emphasizing the role of human-associated VF in microbial survival, informing sterilization practices and microbial management in similar oligotrophic settings beyond spacecraft assembly cleanrooms such as pharmaceutical and medical industry cleanrooms.