Rinke, Christian

Abstract Anthropogenic influences have drastically increased nutrient concentrations in many estuaries globally, and microbial communities have adapted to the resulting hypereutrophic ecosystems. However, our knowledge of the dominant microbial taxa and their potential functions in these ecosystems has remained sparse. Here, we study prokaryotic community dynamics in a temporal–spatial dataset, from a subtropical hypereutrophic estuary. Screening 54 water samples across brackish to marine sites revealed that nutrient concentrations and salinity best explained spatial community variations, whereas temperature and dissolved oxygen likely drive seasonal shifts. By combining short and long read sequencing data, we recovered 2,459 metagenome-assembled genomes, proposed new taxon names for previously uncharacterised lineages, and created an extensive, habitat specific genome reference database. Community profiling based on this genome reference database revealed a diverse prokaryotic community comprising 61 bacterial and 18 archaeal phyla, and resulted in an improved taxonomic resolution at lower ranks down to genus level. We found that the vast majority (61 out of 73) of abundant genera (>1% average) represented unnamed and novel lineages, and that all genera could be clearly separated into brackish and marine ecotypes with inferred habitat specific functions. Applying supervised machine learning and metabolic reconstruction, we identified several microbial indicator taxa responding directly or indirectly to elevated nitrate and total phosphorus concentrations. In conclusion, our analysis highlights the importance of improved taxonomic resolution, sheds light on the role of previously uncharacterised lineages in estuarine nutrient cycling, and identifies microbial indicators for nutrient levels crucial in estuary health assessments.

Abstract The Genome Taxonomy Database (GTDB) is a taxonomic framework that defines prokaryotic taxa as monophyletic groups in concatenated protein reference trees according to systematic criteria. This has resulted in a substantial number of changes to existing classifications (https://gtdb.ecogenomic.org). In the case of union of taxa, GTDB names were applied based on the priority of publication. The division of taxa or change in rank led to the formation of new Latin names above the rank of genus that were only made publicly available via the GTDB website without associated published taxonomic descriptions. This has sometimes led to confusion in the literature and databases. A number of the provisional GTDB names were later published in other studies, while many still lack authorships. To reduce further confusion, here we propose names and descriptions for 329 GTDB-defined prokaryotic taxa, 223 of which are suitable for validation under the International Code of Nomenclature of Prokaryotes (ICNP) and 49 under the Code of Nomenclature of Prokaryotes Described from Sequence Data (SeqCode). For the latter we designated 23 genomes as type material. An additional 57 taxa that do not currently satisfy the validation criteria of either code are proposed as Candidatus.

AbstractAsgardarchaeota have been proposed as the closest living relatives to eukaryotes, and a total of 72 metagenome-assembled genomes (MAGs) representing six primary lineages in this archaeal phylum have thus far been described. These organisms are predicted to be fermentative heterotrophs contributing to carbon cycling in sediment ecosystems. Here, we double the genomic catalogue of Asgardarchaeota by obtaining 71 MAGs from a range of habitats around the globe, including the deep subsurface, brackish shallow lakes, and geothermal spring sediments. Phylogenomic inferences followed by taxonomic rank normalisation confirmed previously established Asgardarchaeota classes and revealed four additional lineages, two of which were consistently recovered as monophyletic classes. We therefore propose the names Candidatus Sifarchaeia class nov. and Ca. Jordarchaeia class nov., derived from the gods Sif and Jord in Norse mythology. Metabolic inference suggests that both classes represent hetero-organotrophic acetogens, which also have the ability to utilise methyl groups such as methylated amines, with acetate as the probable end product in remnants of a methanogen-derived core metabolism. This inferred mode of energy conservation is predicted to be enhanced by genetic code expansions, i.e., stop codon recoding, allowing the incorporation of the rare 21st and 22nd amino acids selenocysteine (Sec) and pyrrolysine (Pyl). We found Sec recoding in Jordarchaeia and all other Asgardarchaeota classes, which likely benefit from increased catalytic activities of Sec-containing enzymes. Pyl recoding, on the other hand, is restricted to Sifarchaeia in the Asgardarchaeota, making it the first reported non-methanogenic archaeal lineage with an inferred complete Pyl machinery, likely providing members of this class with an efficient mechanism for methylamine utilisation. Furthermore, we identified enzymes for the biosynthesis of ester-type lipids, characteristic of bacteria and eukaryotes, in both newly described classes, supporting the hypothesis that mixed ether-ester lipids are a shared feature among Asgardarchaeota.

AbstractThe recently discovered DPANN archaea are a potentially deep-branching, monophyletic radiation of organisms with small cells and genomes. However, the monophyly and early emergence of the various DPANN clades and their role in life’s evolution are debated. Here, we reconstructed and analysed genomes of an uncharacterized archaeal phylum (CandidatusUndinarchaeota), revealing that its members have small genomes and, while potentially being able to conserve energy through fermentation, likely depend on partner organisms for the acquisition of certain metabolites. Our phylogenomic analyses robustly place Undinarchaeota as an independent lineage between two highly supported ‘DPANN’ clans. Further, our analyses suggest that DPANN have exchanged core genes with their hosts, adding to the difficulty of placing DPANN in the tree of life. This pattern can be sufficiently dominant to allow identifying known symbiont-host clades based on routes of gene transfer. Together, our work provides insights into the origins and evolution of DPANN and their hosts.

Abstract 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 Poseidoniales (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.