Stott, Matthew B.

AbstractIn the ongoing debates about eukaryogenesis—the series of evolutionary events leading to the emergence of the eukaryotic cell from prokaryotic ancestors—members of the Asgard archaea play a key part as the closest archaeal relatives of eukaryotes1. However, the nature and phylogenetic identity of the last common ancestor of Asgard archaea and eukaryotes remain unresolved2–4. Here we analyse distinct phylogenetic marker datasets of an expanded genomic sampling of Asgard archaea and evaluate competing evolutionary scenarios using state-of-the-art phylogenomic approaches. We find that eukaryotes are placed, with high confidence, as a well-nested clade within Asgard archaea and as a sister lineage to Hodarchaeales, a newly proposed order within Heimdallarchaeia. Using sophisticated gene tree and species tree reconciliation approaches, we show that analogous to the evolution of eukaryotic genomes, genome evolution in Asgard archaea involved significantly more gene duplication and fewer gene loss events compared with other archaea. Finally, we infer that the last common ancestor of Asgard archaea was probably a thermophilic chemolithotroph and that the lineage from which eukaryotes evolved adapted to mesophilic conditions and acquired the genetic potential to support a heterotrophic lifestyle. Our work provides key insights into the prokaryote-to-eukaryote transition and a platform for better understanding the emergence of cellular complexity in eukaryotic cells.

AbstractTrace metals have been an important ingredient for life throughout Earth’s history. Here, we describe the genome-guided cultivation of a member of the elusive archaeal lineage Caldarchaeales (syn. Aigarchaeota), Wolframiiraptor gerlachensis, and its growth dependence on tungsten. A metagenome-assembled genome (MAG) of W. gerlachensis encodes putative tungsten membrane transport systems, as well as pathways for anaerobic oxidation of sugars probably mediated by tungsten-dependent ferredoxin oxidoreductases that are expressed during growth. Catalyzed reporter deposition-fluorescence in-situ hybridization (CARD-FISH) and nanoscale secondary ion mass spectrometry (nanoSIMS) show that W. gerlachensis preferentially assimilates xylose. Phylogenetic analyses of 78 high-quality Wolframiiraptoraceae MAGs from terrestrial and marine hydrothermal systems suggest that tungsten-associated enzymes were present in the last common ancestor of extant Wolframiiraptoraceae. Our observations imply a crucial role for tungsten-dependent metabolism in the origin and evolution of this lineage, and hint at a relic metabolic dependence on this trace metal in early anaerobic thermophiles.

An aerobic, saccharolytic, obligately thermophilic, motile, non-spore-forming bacterium, strain T49T, was isolated from geothermally heated soil at Hell’s Gate, Tikitere, New Zealand. On the basis of 16S rRNA gene sequence similarity, T49T is the first representative of a new class in the newly described phylum Armatimonadetes, formerly known as candidate division OP10. Cells of strain T49T stained Gram-negative and were catalase-positive and oxidase-negative. Cells possessed a highly corrugated outer membrane. The major fatty acids were 16 : 0, i17 : 0 and ai17 : 0. The G+C content of the genomic DNA was 54.6 mol%. Strain T49T grew at 50–73 °C with an optimum temperature of 68 °C, and at pH 4.7–5.8 with an optimum growth pH of 5.3. A growth rate of 0.012 h−1 was observed under optimal temperature and pH conditions. The primary respiratory quinone was MK-8. Optimal growth was achieved in the absence of NaCl, although growth was observed at NaCl concentrations as high as 2 % (w/v). Strain T49T was able to utilize mono- and disaccharides such as cellobiose, lactose, mannose and glucose, as well as branched or amorphous polysaccharides such as starch, CM-cellulose, xylan and glycogen, but not highly linear polysaccharides such as crystalline cellulose or cotton. On the basis of its phylogenetic position and phenotypic characteristics, we propose that strain T49T represents a novel bacterial genus and species within the new class Chthonomonadetes classis nov. of the phylum Armatimonadetes. The type strain of Chthonomonas calidirosea gen. nov., sp. nov. is T49T ( = DSM 23976T = ICMP 18418T).