Archaea and the origin of eukaryotes

  • A Corrigendum to this article was published on 27 November 2017

Key Points

  • The Archaea was recognized as a third domain of life 40 years ago. Molecular evidence soon suggested that the Eukarya represented a sister group to the Archaea or that eukaryotes descended from archaea.

  • Culture-independent genomics has revealed the vast diversity existing among the Archaea, including the recently described Asgard superphylum. Phylogenomic analyses have placed the Asgard archaea as the closest prokaryotic relatives of eukaryotes.

  • Comparative genomic analyses have reconstructed a complex last eukaryotic common ancestor. However, how and in which order these complex eukaryotic features evolved in an Asgard archaea-related ancestor remains largely unclear.

  • Genomic investigation of Asgard archaea showed that they carry several genes formerly believed to be eukaryotic specific, illuminating early events during eukaryogenesis.

  • Fully understanding the process of eukaryogenesis requires finding answers to several challenging and intertwined questions. Although we have seemingly answered some of these questions, others remain fiercely debated, and new questions continue to arise.

Abstract

Woese and Fox's 1977 paper on the discovery of the Archaea triggered a revolution in the field of evolutionary biology by showing that life was divided into not only prokaryotes and eukaryotes. Rather, they revealed that prokaryotes comprise two distinct types of organisms, the Bacteria and the Archaea. In subsequent years, molecular phylogenetic analyses indicated that eukaryotes and the Archaea represent sister groups in the tree of life. During the genomic era, it became evident that eukaryotic cells possess a mixture of archaeal and bacterial features in addition to eukaryotic-specific features. Although it has been generally accepted for some time that mitochondria descend from endosymbiotic alphaproteobacteria, the precise evolutionary relationship between eukaryotes and archaea has continued to be a subject of debate. In this Review, we outline a brief history of the changing shape of the tree of life and examine how the recent discovery of a myriad of diverse archaeal lineages has changed our understanding of the evolutionary relationships between the three domains of life and the origin of eukaryotes. Furthermore, we revisit central questions regarding the process of eukaryogenesis and discuss what can currently be inferred about the evolutionary transition from the first to the last eukaryotic common ancestor.

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Figure 1: Evolution of the tree of life.
Figure 2: Genomic exploration of TACK and Asgard archaeal diversity.
Figure 3: Key time points in eukaryogenesis.
Figure 4: Evolutionary scenarios for the origins of bacterial genes in eukaryotes.
Figure 5: Origins of eukaryotic signature proteins present in FECA.

Change history

  • 27 November 2017

    On pages 714–715 of this article, in the first paragraph of the section What do we currently know about LECA?, the sentence “Phylogenomic and comparative genomic analyses have led to the hypothesis that LECA, estimated to have lived 1–1.9 million years ago54, already was a fully fledged eukaryote and possessed a large number of features that are uniquely found in modern eukaryotes55,56.” should have read “Phylogenomic and comparative genomic analyses have led to the hypothesis that LECA, estimated to have lived 1–1.9 billion years ago54, already was a fully fledged eukaryote and possessed a large number of features that are uniquely found in modern eukaryotes55,56.” This has been corrected in the online version of the article. The authors apologize to the readers for any misunderstanding caused.

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Acknowledgements

The authors wish to thank A. Roger and W. F. Doolittle for fruitful discussions. L.E. is funded by the European Union's Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No 704263. J.L. is supported by a postdoctoral fellowship for foreign researchers from the Wenner-Gren Foundations in Stockholm (UPD2016-0072). C.W.S. is supported by a European Molecular Biology Organization long-term fellowship (ALTF-997-2015) and the Natural Sciences and Engineering Research Council of Canada postdoctoral research fellowship (PDF-487174-2016). This work is supported by grants of the European Research Council (ERC Starting Grant 310039-PUZZLE_CELL), the Swedish Foundation for Strategic Research (SSF-FFL5) and the Swedish Research Council (VR grant 2015–04959), awarded to T.J.G.E.

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L.E., A.S., J.L., C.W.S. and T.J.G.E. researched data for the article. L.E., A.S., J.L., C.W.S. and T.J.G.E. substantially contributed to the discussion of content. L.E., A.S., J.L. and T.J.G.E. wrote the article. L.E., A.S., J.L., C.W.S. and T.J.G.E. reviewed and edited the manuscript before submission.

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Correspondence to Thijs J. G. Ettema.

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Glossary

Sister groups

Two descendants that split from the same node; the descendants are each other's closest relative.

Monophyletic groups

A monophyletic group is a group of organisms that forms a clade, which consists of all the descendants of a common ancestor.

Eukaryogenesis

The whole sequence of evolutionary events occurring between the first eukaryotic common ancestor (FECA) and the last eukaryotic common ancestor (LECA) explaining the process by which eukaryotic cells evolved from prokaryotic ancestors.

Metagenomics

The sequencing of genetic material extracted directly from environmental samples.

Genome-resolved metagenomics

The assembly of complete or draft genomes exclusively from metagenomic sequencing data.

DPANN

A proposed archaeal superphylum comprising Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanohaloarchaeota and Nanoarchaeota. More recently, it was suggested that additional candidate phyla such as Woesearchaeota, Pacearchaeota, Micrarchaeota and possibly Altiarchaeales are part of this group.

Hydrothermal vents

Areas of the sea floor from which geothermally heated water issues.

Eukaryotic signature proteins

(ESPs). Proteins involved in key eukaryotic processes and conserved across most eukaryotic diversity.

First eukaryotic common ancestor

(FECA). The most ancient organism whose only living descendants are present-day eukaryotes.

Last eukaryotic common ancestor

(LECA). The most recent ancestor of all present-day eukaryotes.

Telomeres

Repetitive nucleotide sequences located at the ends of the linear chromosomes of most eukaryotic organisms.

Spliceosomal introns

Introns in the nuclear protein-coding genes of eukaryotes that are removed by spliceosomes.

Proteasome

A large protein complex responsible for regulated degradation of proteins as part of the ubiquitin system found in all eukaryotes.

Horizontal gene transfer

(HGT). Exchange of genetic material between cells and/or organisms; sometimes called lateral gene transfer. This contrasts with the vertical inheritance of DNA from parent to offspring.

Genomic streamlining

A form of genome evolution that occurs through size reduction and simplification in terms of gene content; particularly common among parasitic organisms.

Phylogenetic signal

Information contained in homologous molecular sequences used to reconstruct the historical relationships between the sequences.

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Eme, L., Spang, A., Lombard, J. et al. Archaea and the origin of eukaryotes. Nat Rev Microbiol 15, 711–723 (2017). https://doi.org/10.1038/nrmicro.2017.133

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