Recent advances in phylogenomic analyses and increased genomic sampling of uncultured prokaryotic lineages have brought compelling evidence in support of the emergence of eukaryotes from within the archaeal domain of life (eocyte hypothesis)1,2. The discovery of Asgardarchaeota and its supposed position at the base of the eukaryotic tree of life3,4 provided cues about the long-awaited identity of the eocytic lineage from which the nucleated cells (Eukaryota) emerged. While it is apparent that Asgardarchaeota encode a plethora of eukaryotic-specific proteins (the highest number identified yet in prokaryotes)5, the lack of genomic information and metabolic characterization has precluded inferences about their lifestyles and the metabolic landscape that favoured the emergence of the protoeukaryote ancestor. Here, we use advanced phylogenetic analyses for inferring the deep ancestry of eukaryotes, and genome-scale metabolic reconstructions for shedding light on the metabolic milieu of Asgardarchaeota. In doing so, we: (1) show that Heimdallarchaeia (the closest eocytic lineage to eukaryotes to date) are likely to have a microoxic niche, based on their genomic potential, with aerobic metabolic pathways that are unique among Archaea (that is, the kynurenine pathway); (2) provide evidence of mixotrophy within Asgardarchaeota; and (3) describe a previously unknown family of rhodopsins encoded within the recovered genomes.

Department of Aquatic Microbial Ecology Institute of Hydrobiology Biology Centre of the Academy of Sciences of the Czech Republic České Budějovice Czech Republic

Department of Life Science and Applied Chemistry Nagoya Institute of Technology Nagoya Japan

Department of Molecular Biology and Biotechnology Faculty of Biology and Geology Babeş Bolyai University Cluj Napoca Romania

Faculty of Biology Technion Israel Institute of Technology Haifa Israel

Limnological Station Institute of Plant and Microbial Biology University of Zurich Kilchberg Switzerland

Molecular Biology Center Institute for Interdisciplinary Research in Bio Nano Sciences Babeş Bolyai University Cluj Napoca Romania

The Institute for Solid State Physics The University of Tokyo Kashiwa Japan

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Nat Microbiol. 2019 Jul;4(7):1068-1070. doi: 10.1038/s41564-019-0495-5. PubMed

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Cox, C. J., Foster, P. G., Hirt, R. P., Harris, S. R. & Embley, T. M. The archaebacterial origin of eukaryotes. Proc. Natl Acad. Sci. USA 105, 20356–20361 (2008). DOI

Williams, T. A., Foster, P. G., Cox, C. J. & Embley, T. M. An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504, 231–236 (2013). DOI

Spang, A. et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521, 173–179 (2015). DOI

Spang, A. et al. Asgard archaea are the closest prokaryotic relatives of eukaryotes. PLoS Genet. 14, e1007080 (2018). DOI

Zaremba-Niedzwiedzka, K. et al. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541, 353–358 (2017). DOI

McInerney, J. O., O’Connell, M. J. & Pisani, D. The hybrid nature of the Eukaryota and a consilient view of life on Earth. Nat. Rev. Microbiol. 12, 449–455 (2014). DOI

Da Cunha, V., Gaia, M., Nasir, A. & Forterre, P. Asgard archaea do not close the debate about the universal tree of life topology. PLoS Genet. 14, e1007215 (2018). DOI

de Duve, C. The origin of eukaryotes: a reappraisal. Nat. Rev. Genet. 8, 395–403 (2007). DOI

Lake, J. A., Henderson, E., Oakes, M. & Clark, M. W. Eocytes: a new ribosome structure indicates a kingdom with a close relationship to eukaryotes. Proc. Natl Acad. Sci. USA 81, 3786–3790 (1984). DOI

Woese, C. R., Kandler, O. & Wheelis, M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA 87, 4576–4579 (1990). DOI

Eme, L., Spang, A., Lombard, J., Stairs, C. W. & Ettema, T. J. G. Archaea and the origin of eukaryotes. Nat. Rev. Microbiol. 15, 711–723 (2017). DOI

Martijn, J., Vosseberg, J., Guy, L., Offre, P. & Ettema, T. J. G. Deep mitochondrial origin outside the sampled alphaproteobacteria. Nature 557, 101–105 (2018). DOI

Susko, E. & Roger, A. J. On reduced amino acid alphabets for phylogenetic inference. Mol. Biol. Evol. 24, 2139–2150 (2007). DOI

Liu, Y. et al. Comparative genomic inference suggests mixotrophic lifestyle for Thorarchaeota. ISME J. 12, 1021–1031 (2018). DOI

Dodding, M. P. Folliculin—a tumor suppressor at the intersection of metabolic signaling and membrane traffic. Small GTPases 8, 100–105 (2017). DOI

Pushkarev, A. et al. A distinct abundant group of microbial rhodopsins discovered using functional metagenomics. Nature 558, 595–599 (2018). DOI

Flores-Uribe, J. Heliorhodopsins are absent in diderm (Gram-negative) bacteria: Some thoughts and possible implications for activity. Environ. Microbiol. Rep. https://doi.org/10.1111/1758-2229.12730 (2019). DOI

Petrovskaya, L. E. et al. Predicted bacteriorhodopsin from Exiguobacterium sibiricum is a functional proton pump. FEBS Lett. 584, 4193–4196 (2010). DOI

Alexe, M. Studiul Lacurilor Sărate din Depresiunea Transilvaniei (Presa Universitară Clujeană, Cluj-Napoca, 2010).

Sousa, F. L., Neukirchen, S., Allen, J. F., Lane, N. & Martin, W. F. Lokiarchaeon is hydrogen dependent. Nat. Microbiol. 1, 16034 (2016). DOI

Ternes, C. M. & Schönknecht, G. Gene transfers shaped the evolution of de novo NAD DOI

Gazzaniga, F., Stebbins, R., Chang, S. Z., McPeek, M. A. & Brenner, C. Microbial NAD metabolism: lessons from comparative genomics. Microbiol. Mol. Biol. Rev. 73, 529–541 (2009). DOI

Kurnasov, O. et al. Aerobic tryptophan degradation pathway in bacteria: novel kynurenine formamidase. FEMS Microbiol. Lett. 227, 219–227 (2003). DOI

Abaibou, H., Pommier, J., Benoit, S., Giordano, G. & Mandrand-Berthelot, M. A. Expression and characterization of the Escherichia coli fdo locus and a possible physiological role for aerobic formate dehydrogenase. J. Bacteriol. 177, 7141–7149 (1995). DOI

Brasen, C., Esser, D., Rauch, B. & Siebers, B. Carbohydrate metabolism in Archaea: current insights into unusual enzymes and pathways and their regulation. Microbiol. Mol. Biol. Rev. 78, 89–175 (2014). DOI

Dorr, C., Zaparty, M., Tjaden, B., Brinkmann, H. & Siebers, B. The hexokinase of the hyperthermophile Thermoproteus tenax. ATP-dependent hexokinases and ADP-dependent glucokinases, two alternatives for glucose phosphorylation in Archaea. J. Biol. Chem. 278, 18744–18753 (2003). DOI

Kono, T. et al. A RuBisCO-mediated carbon metabolic pathway in methanogenic archaea. Nat. Commun. 8, 14007 (2017). DOI

Techtmann, S. M. et al. Evidence for horizontal gene transfer of anaerobic carbon monoxide dehydrogenases. Front. Microbiol. 3, 132 (2012). DOI

Martin, W. F. Hydrogen, metals, bifurcating electrons, and proton gradients: The early evolution of biological energy conservation. FEBS Lett. 586, 485–493 (2012). DOI

Betts, H. et al. Integrated genomic and fossil evidence illuminates life’s early evolution and eukaryote origins. Nat. Ecol. Evol. 2, 1556–1562 (2018). DOI

Gastescu, P. & Teodorescu, D. C. The lakes of the Romanian Black Sea coast. man-induced changes, water regime, present state. Rom. J. Geogr. 60, 27–42 (2016).

Fedorov, P. V. Postglacial transgression of the Black Sea. Int. Geol. Rev. 14, 160–164 (1972). DOI

Bushnell, B., Rood, J. & Singer, E. BBMerge—accurate paired shotgun read merging via overlap. PLoS ONE 12, e0185056 (2017). DOI

Bushnell, B. BBMap short read aligner, and other bioinformatic tools. SourceForge https://sourceforge.net/projects/bbmap (2016).

Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010). DOI

Pruesse, E. et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35, 7188–7196 (2007). DOI

Nawrocki, E. P. Structural RNA Homology Search and Alignment using Covariance Models. PhD thesis, Washington Univ. School of Medicine (2009).

Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990). DOI

Li, D., Liu, C.-M., Luo, R., Sadakane, K. & Lam, T.-W. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31, 1674–1676 (2015). DOI

Hyatt, D., LoCascio, P. F., Hauser, L. J. & Uberbacher, E. C. Gene and translation initiation site prediction in metagenomic sequences. Bioinformatics 28, 2223–2230 (2012). DOI

Steinegger, M. & Söding, J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat. Biotechnol. 35, 1026 (2017). DOI

Kang, D. D., Froula, J., Egan, R. & Wang, Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ 3, e1165 (2015). DOI

Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015). DOI

Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014). DOI

Kanehisa, M., Sato, Y. & Morishima, K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J. Mol. Biol. 428, 726–731 (2016). DOI

Lowe, T. M. & Eddy, S. R. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955–964 (1997). DOI

Makarova, K. S., . & Wolf, Y. I. & Koonin, E. V. Archaeal clusters of orthologous genes (arcogs): an update and application for analysis of shared features between thermococcales, methanococcales, and methanobacteriales. Life 5, 818–840 (2015). DOI

Jones, P. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014). DOI

Finn, R. D. et al. HMMER web server: 2015 update. Nucleic Acids Res. 43, W30–W38 (2015). DOI

Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Sternberg, M. J. E. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10, 845–858 (2015). DOI

Käll, L., Krogh, A. & Sonnhammer, E. L. L. Advantages of combined transmembrane topology and signal peptide prediction—the Phobius web server. Nucleic Acids Res. 35, W429–W432 (2007). DOI

Loytynoja, A. Phylogeny-aware alignment with PRANK. Methods Mol. Biol. 1079, 155–170 (2014). DOI

Criscuolo, A. & Gribaldo, S. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol. Biol. 10, 210 (2010). DOI

Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: Improving the Ultrafast Bootstrap Approximation. Mol. Biol. Evol. 35, 518–522 (2018). DOI

Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015). DOI

Lartillot, N., Rodrigue, N., Stubbs, D. & Richer, J. PhyloBayes MPI: phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment. Syst. Biol. 62, 611–615 (2013). DOI

Notredame, C., Higgins, D. G. & Heringa, J. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205–217 (2000). DOI

Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004). DOI

Tabita, F. R. et al. Function, structure, and evolution of the RubisCO-like proteins and their RubisCO homologs. Microbiol. Mol. Biol. Rev. 71, 576–599 (2007). DOI

Wrighton, K. C. et al. RubisCO of a nucleoside pathway known from Archaea is found in diverse uncultivated phyla in bacteria. ISME J. 10, 2702–2714 (2016). DOI

Castro-Fernandez, V. et al. Reconstructed ancestral enzymes reveal that negative selection drove the evolution of substrate specificity in ADP-dependent kinases. J. Biol. Chem. 292, 21218 (2017). DOI

Katoh, K. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002). DOI

Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010). DOI

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Common Presence of Phototrophic Gemmatimonadota in Temperate Freshwater Lakes

Expanded Diversity and Metabolic Versatility of Marine Nitrite-Oxidizing Bacteria Revealed by Cultivation- and Genomics-Based Approaches

Visualization of Lokiarchaeia and Heimdallarchaeia (Asgardarchaeota) by Fluorescence In Situ Hybridization and Catalyzed Reporter Deposition (CARD-FISH)

Schizorhodopsins: A family of rhodopsins from Asgard archaea that function as light-driven inward H+ pumps