Universal Tree of Life

Abstract

The first tree of life based on the comparison of ribosomal RNA (ribonucleic acid) allowed classifying all ribosome‐encoding organisms into three domains: Archaea, Bacteria and Eukarya. Phylogenomics analyses later on show that these domains probably emerged from a last universal common ancestor (LUCA) simpler than modern organisms. Different results are however still obtained regarding the relationships between Archaea and Eukarya when relying on concatenations of universal proteins. Recent analyses have revealed that the topology obtained in these studies is strongly dependent on the universal proteins and species data sets. On the basis of this observation, our recent phylogenetic analyses presently support the sisterhood of Archaea and Eukarya. Viruses, defined as virion‐encoding organisms, cannot be formally located in the tree of life but populate it entirely from its trunk to the leaves.

Key Concepts

  • Ribosome‐encoding organisms have been classified into three domains based on their 16S ribosomal RNA sequences.
  • The last universal common ancestor (LUCA) was probably much simpler than modern organisms.
  • The tree of life can be theoretically determined from the phylogenetic analysis of universal proteins.
  • Different universal proteins strongly favour opposite scenarios for the origin of eukaryotes.
  • The addition of fast‐evolving organisms to species data sets favours the branching of eukaryotes within archaea.
  • Phylogenies of RNA polymerases, the largest universal proteins, support the monophyly of the three domains and the sisterhood of Archaea and Eukarya.
  • Viruses cannot be formally located in the universal tree of life, but infect the universal tree from the trunk to the leaves.

Keywords: tree of life; LUCA; Archaea; Bacteria; origin of eukaryotes; virus evolution

Figure 1. (a) Venn diagram representing the number of shared or specific ribosomal subunits in the ribosomes of the three domains. (b) Hypothesis of distribution of the r‐proteins along the evolution of the ribosomes, from LUCA to the three cellular domains.
Figure 2. Some specific molecular features that originated in the different branches of the universal tree of life.
Figure 3. (a) Schematic representation of an eocyte tree of life. (b) Schematic representation of a Woese tree of life.
close

References

Abrescia NG, Bamford DH, Grimes JM and Stuart DI (2012) Structure unifies the viral universe. Annual Review of Biochemistry 81: 795–822.

Adam PS, Borrel G and Gribaldo S (2018) Evolutionary history of carbon monoxide dehydrogenase/acetyl‐CoA synthase, one of the oldest enzymatic complexes. Proceedings of the National Academy of Sciences of the United States of America 115 (6): E1166–E1173.

Baker BJ, Comolli LR, Dick GJ, et al. (2010) Enigmatic, ultrasmall, uncultivated Archaea. Proceedings of the National Academy of Sciences of the United States of America 107 (19): 8806–8811.

Bamford DH (2003) Do viruses form lineages across different domains of life? Research in Microbiology 154 (4): 231–236.

Bengtson S, Rasmussen B, Ivarsson M, et al. (2017) Fungus‐like mycelial fossils in 2.4‐billion‐year‐old vesicular basalt. Nature Ecology & Evolution 1 (6): 141. DOI: 10.1038/s41559-017-0141.

Boussau B, Blanquart S, Necsulea A, Lartillot N and Gouy M (2008) Parallel adaptations to high temperatures in the Archaean eon. Nature 456 (7224): 942–945.

Boyer M, Madoui M‐A, Gimenez G, La Scola B and Raoult D (2010) Phylogenetic and phyletic studies of informational genes in genomes highlight existence of a 4th domain of life including giant viruses. PLoS One 5 (12): e15530.

Brochier‐Armanet C and Forterre P (2007) Widespread distribution of archaeal reverse gyrase in thermophilic bacteria suggests a complex history of vertical inheritance and lateral gene transfers. Archaea 2 (2): 83–93.

Brown JR and Doolittle WF (1997) Archaea and the prokaryote‐to‐eukaryote transition. Microbiology and Molecular Biology Reviews 61 (4): 456–502.

Chang J, Nie X, Chang HE, Han Z and Taylor J (2008) Transcription of hepatitis delta virus RNA by RNA polymerase II. Journal of Virology 82 (3): 1118–1127.

Cox CJ, Foster PG, Hirt RP, Harris SR and Embley TM (2008) The archaebacterial origin of eukaryotes. Proceedings of the National Academy of Sciences of the United States of America 105 (51): 20356–20361.

Da Cunha V, Gaia M, Gadelle D, Nasir A and Forterre P (2017) Lokiarchaea are close relatives of Euryarchaeota, not bridging the gap between prokaryotes and eukaryotes. PLoS Genetics 13 (6): e1006810.

Da Cunha V, Gaia M, Nasir A and Forterre P (2018) Asgard archaea do not close the debate about the universal tree of life topology. PLoS Genetics 14 (3): e1007215.

El Albani A, Bengtson S, Canfield DE, et al. (2010) Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago. Nature 466 (7302): 100–104.

Forterre P (1995) Thermoreduction, a hypothesis for the origin of prokaryotes. Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie 318 (4): 415–422.

Forterre P and Philippe H (1999) Where is the root of the universal tree of life? BioEssays 21 (10): 871–879.

Forterre P (2006) Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain. Proceedings of the National Academy of Sciences of the United States of America 103 (10): 3669–3674.

Forterre P and Gadelle D (2009) Phylogenomics of DNA topoisomerases: their origin and putative roles in the emergence of modern organisms. Nucleic Acids Research 37 (3): 679–692.

Forterre P (2012) Virocell concept, The. In: eLS. Chichester: John Wiley & Sons, Ltd. http://www.els.net [DOI: 10.1002/9780470015902.a0023264].

Forterre P (2013) The common ancestor of Archaea and Eukarya was not an archaeon. Archaea 2013: Article ID 372396. DOI: 10.1155/2013/372396.

Forterre P, Krupovic M and Prangishvili D (2014) Cellular domains and viral lineages. Trends in Microbiology 22 (10): 554–558.

Forterre P (2015) The universal tree of life: an update. Frontiers in Microbiology 6: 717. DOI: 10.3389/fmicb.2015.00717.

Forterre P (2016) To be or not to be alive: how recent discoveries challenge the traditional definitions of viruses and life. Studies in History and Philosophy of Biological and Biomedical Sciences 59: 100–108.

Garnier F, Debat H and Nadal M (2018) Type IA DNA Topoisomerases: a universal core and multiple activities. Methods in Molecular Biology 1703: 1–20. DOI: 10.1007/978-1-4939-7459-7_1.

Gogarten JP, Kibak H, Dittrich P, et al. (1989) Evolution of the vacuolar H+‐ATPase: implications for the origin of eukaryotes. Proceedings of the National Academy of Sciences of the United States of America 86 (17): 6661–6665.

Gouy M, Baurain D and Philippe H (2015) Rooting the tree of life: the phylogenetic jury is still out. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 370 (1678): 20140329.

Gribaldo S, Poole AM, Daubin V, Forterre P and Brochier‐Armanet C (2010) The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? Nature Reviews Microbiology 8 (10): 743–752.

Grosjean H, Marck C and de Crécy‐Lagard V (2007) The various strategies of codon decoding in organisms of the three domains of life: evolutionary implications. Nucleic Acids Symposium Series 51: 15–16.

Groussin M and Gouy M (2011) Adaptation to environmental temperature is a major determinant of molecular evolutionary rates in archaea. Molecular Biology and Evolution 28: 2661–2674.

Guy L and Ettema TJG (2011) The archaeal ‘TACK’ superphylum and the origin of eukaryotes. Trends in Microbiology 19 (12): 580–587.

Hug LA, Baker BJ, Anantharaman K, et al. (2016) A new view of the tree of life. Nature Microbiology 11 (1): 16048.

Iwabe N, Kuma K, Hasegawa M, Osawa S and Miyata T (1989) Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proceedings of the National Academy of Sciences of the United States of America 86 (23): 9355–9359.

Koonin EV (2010) The incredible expanding ancestor of eukaryotes. Cell 140 (5): 606–608.

Krupovic M and Bamford DH (2010) Order to the viral universe. Journal of Virology 84 (24): 12476–12479.

Krupovic M and Koonin EV (2017) Multiple origins of viral capsid proteins from cellular ancestors. Proceedings of the National Academy of Sciences of the United States of America 114 (12): E2401–E2410. DOI: 10.1073/pnas.1621061114.

Kurland CG, Collins LJ and Penny D (2006) Genomics and the irreducible nature of eukaryote cells. Science 312 (5776): 1011–1014.

Lake JA (1988) Origin of the eukaryotic nucleus determined by rate‐invariant analysis of rRNA sequences. Nature 331 (6152): 184–186.

Lane N and Martin W (2010) The energetics of genome complexity. Nature 467 (7318): 929–934.

Lecompte O, Ripp R, Thierry JC, Moras D and Poch O (2002) Comparative analysis of ribosomal proteins in complete genomes: an example of reductive evolution at the domain scale. Nucleic Acids Research 30 (24): 5382–5390.

Moreira D and López‐García P (2009) Ten reasons to exclude viruses from the tree of life. Nature Reviews Microbiology 7 (4): 306–311.

Mulkidjanian AY, Makarova KS, Galperin MY and Koonin EV (2007) Inventing the dynamo machine: the evolution of the F‐type and V‐type ATPases. Nature Reviews Microbiology 5 (11): 892–899.

Nasir A, Kim KM, Da Cunha V and Caetano‐Anollés G (2016) Arguments reinforcing the three‐domain view of diversified cellular life. Archaea 2016: Article ID 1851865. DOI: 10.1155/2016/1851865.

Pittis AA and Gabaldón T (2016) Late acquisition of mitochondria by a host with chimaeric prokaryotic ancestry. Nature 531 (7592): 101–104.

Raoult D and Forterre P (2008) Redefining viruses: lessons from Mimivirus. Nature Reviews Microbiology 6 (4): 315–319.

Raymann K, Brochier‐Armanet C and Gribaldo S (2015) The two‐domain tree of life is linked to a new root for the Archaea. Proceedings of the National Academy of Sciences of the United States of America 112 (21): 6670–6675.

Shen X, Hittinger CT and Rokas A (2017) Studies can be driven by a handful of genes. Nature Ecology & Evolution 1 (5): 126. DOI: 10.1038/s41559-017-0126.

Spang A, Saw JH, Jørgensen S, et al. (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521 (7551): 173–179.

Spang A, Eme L, Saw J, et al. (2018) Asgard archaea are the closest prokaryotic relatives of eukaryotes. PLoS Genetics 14 (3): e1007080.

Werner F and Grohmann D (2011) Evolution of multisubunit RNA polymerases in the three domains of life. Nature Reviews Microbiology 9 (2): 85–98.

Williams TA, Szöllösi GJ, Spang A, et al. (2017) Integrative modeling of gene and genome evolution roots the archaeal tree of life. Proceedings of the National Academy of Sciences of the United States of America 114 (23): E4602–E4611. DOI: 10.1073/pnas.1618463114.

Woese CR and Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proceedings of the National Academy of Sciences of the United States of America 74 (11): 5088–5090.

Woese CR, Kandler O and Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proceedings of the National Academy of Sciences of the United States of America 87 (12): 4576–4579.

Zaremba‐Niedzwiedzka K, Caceres EF, Saw JH, et al. (2017) Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541 (7637): 353–358.

Further Reading

Forterre P (2016) Microbes from Hell. Chicago, IL: University of Chicago Press.

Sapp J and Fox GE (2013) The singular quest for a universal tree of life. Microbiology and Molecular Biology Reviews 77 (4): 541–550.

The Evomobil Project (2017) Archaea of the Putative Asgard Superphylum do not Close the Debate about the Universal Tree of Life Topology. https://www.the‐evomobil‐project.com/single‐post/2017/08/22/Archaea‐of‐the‐putative‐Asgard‐superphylum‐do‐not‐close‐the‐debate‐about‐the‐universal‐tree‐of‐life‐topology

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Forterre, Patrick, Da Cunha, Violette, and Gaïa, Morgan(Jun 2018) Universal Tree of Life. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001525.pub3]