Casting light on Asgardarchaeota metabolism in a sunlit microoxic niche

Abstract

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.

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Fig. 1: Asgardarchaeota phylogenomics.
Fig. 2: Phylogenetic analysis of rhodopsins.
Fig. 3: Metabolic reconstruction of Heimdallarchaeia.
Fig. 4: De novo NAD+ synthesis pathways.

Data availability

Sequence data generated during this study have been deposited in the NCBI Sequence Read Archive (SRA) under study number SRP155597 and linked to BioProject ID PRJNA483005. The Whole Genome Shotgun project containing genome bins assembled in this study has been deposited at DDBJ/ENA/GenBank under the accessions SDMS00000000–SDOA00000000. The versions described in this paper are version SDMS01000000–SDOA01000000. The derived data that support the findings of this paper are available in figshare with the identifier https://doi.org/10.6084/m9.figshare.702262. All other relevant data supporting the findings of this study are available within the paper and its supplementary information files. No custom code that is central to the conclusions of this study was generated. All programs used in data analyses are listed in detail with their version numbers in the Nature Research Reporting Summary linked to this article.

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Acknowledgements

We thank Z. Keresztes, V. Muntean, T. Szőke-Nagy, M. Alexe, A. Cristea and A. Baricz for their technical support during sampling and sample preparation, and E. A. Levei and M. Șenilă for contributions to chemical analyses. P.-A.B was supported by the research grant PN-III-P4-ID-PCE-2016-0303 (Romanian National Authority for Scientific Research). H.L.B. was supported by the research grants PN-III-P4-ID-PCE-2016-0303 (Romanian National Authority for Scientific Research) and STAR-UBB Advanced Fellowship-Intern (Babeș-Bolyai University). A.-Ş.A. was supported by the research grants: 17-04828 S (Grant Agency of the Czech Republic) and MSM200961801 (Academy of Sciences of the Czech Republic). M.M. was supported by the Postdoctoral Programme PPPLZ L200961651 (Academy of Sciences of the Czech Republic). R.G. was supported by the research grant 17-04828 S (Grant Agency of the Czech Republic).

Author information

H.L.B. and P.-A.B. designed the study. P.-A.B., A.-Ş.A. and R.G. wrote the manuscript. P.-A.B., A.-Ş.A., R.G., M.M.S. and M.M. analysed and interpreted the data. R.G., O.B., K.I. and H.K. performed rhodopsin data analyses. All authors commented on and approved the manuscript.

Correspondence to Rohit Ghai.

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Supplementary Information

Supplementary Information

Supplementary Discussion, Supplementary Figures 1–7, Supplementary Table 2, Supplementary Table 5, Supplementary Tables 7–9 and Supplementary References.

Reporting Summary

Supplementary Table 1

General statistics for MAGs recovered from the Amara and Tekirghiol Lakes.

Supplementary Table 3

KEGG orthology annotation for Asgardarchaeota MAGs.

Supplementary Table 4

Taxonomy and gene function assignment for Heimdall_RS678-c45 contig by blastx (default parameters).

Supplementary Table 6

Lineages used for inferring phylogenies.

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