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Review
. 2022 May 31;14(6):evac034.
doi: 10.1093/gbe/evac034.

Evolving Perspective on the Origin and Diversification of Cellular Life and the Virosphere

Anja Spang  1   2 , Tara A Mahendrarajah  1 , Pierre Offre  1 , Courtney W Stairs  3
Affiliations
Review

Evolving Perspective on the Origin and Diversification of Cellular Life and the Virosphere

Anja Spang et al. Genome Biol Evol. .

Abstract

The tree of life (TOL) is a powerful framework to depict the evolutionary history of cellular organisms through time, from our microbial origins to the diversification of multicellular eukaryotes that shape the visible biosphere today. During the past decades, our perception of the TOL has fundamentally changed, in part, due to profound methodological advances, which allowed a more objective approach to studying organismal and viral diversity and led to the discovery of major new branches in the TOL as well as viral lineages. Phylogenetic and comparative genomics analyses of these data have, among others, revolutionized our understanding of the deep roots and diversity of microbial life, the origin of the eukaryotic cell, eukaryotic diversity, as well as the origin, and diversification of viruses. In this review, we provide an overview of some of the recent discoveries on the evolutionary history of cellular organisms and their viruses and discuss a variety of complementary techniques that we consider crucial for making further progress in our understanding of the TOL and its interconnection with the virosphere.

Keywords: archaea; bacteria and eukaryotes; diversity and evolution; eukaryogenesis; methodological progress; tree of life; viruses.

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Figures

Fig. 1.
Fig. 1.
Tree of cellular life (TOL) and connection to the six major realms of viruses. The tree is a schematic representation of the relationship of the major domains of life, comprised of the primary domains of Archaea and Bacteria and the secondary domain of Eukaryota. The assumption that Archaea and Bacteria form separate domains of life is dependent on the placement of the root between those domains, though this hypothesis remains to be validated. Although the node separating the DPANN (acronym referenced in text) from all other archaeal clades has been suggested to be the most ancestral split on the archaeal branch, the CPR (acronym referenced in text) most likely represents a more recently evolved sister-clade of the Chloroflexota (Coleman et al. 2021). Current data support an origin of the eukaryotic cell through a symbiosis between an ancestral member of the Asgard archaea (also Asgardarchaeota) (purple arrow) and Alphaproteobacteria (blue arrow), though the timing of the mitochondrial acquisition is debated and the events leading to LECA are poorly resolved. On the outside of the TOL, we illustrate the connection of the three cellular domains with virus representatives belonging to either of the six major viral realms, the Riboviria, Monodnaviria, Varidnaviria, Duplodnaviria, Adnaviria, and Ribozyviria (Krupovic et al. 2020; Koonin et al. 2021). The latter two realms are restricted to the Archaea or eukaryotes, respectively. The Riboviria have so far only been found associated with Bacteria and eukaryotes, whereas all other realms include members infecting cellular organisms across the TOL. LECA, last eukaryotic common ancestor.
Fig. 2.
Fig. 2.
Schematic representation of the phylogenetic diversity of eukaryotes. Groups with taxonomic rankings of phylum level or higher are shown in black (according to Adl et al. 2019 and references in text). Select lineages or organisms that have been recently discovered and placed in the eukaryotic TOL are shown in bold. Eukaryotic supergroups are colored for clarity. Lineages with one or more representative with a primary (1°) secondary (2°) or complex red (C) plastids are indicated with hexagons based on Sibbald and Archibald (2020). Sar, Stramenopila-Alveolata-Rhizaria; TSAR, Telonemia+SAR (Strassert et al. 2019), CAM (Yazaki et al. 2021), Cryptista-Archaeplastida-Microheiliella maris; “CRuMs,” Collodictyonids, Rigifilida, Mantamonas plastica.
Fig. 3.
Fig. 3.
The diversity of the core virosphere and its links to bacterial, archaeal, and eukaryotic hosts. For each viral realm, we depict the diversity of viral families that have representatives infecting members either the Bacteria, Archaea, or Eukaryota, respectively. Asterisk: for eukaryotic viruses assigned to the Riboviria, we report orders instead of families. The shapes represent a small selection of characteristic morphologies seen within certain viral realms. The information on viral families comprising the various realms is derived from the ICTV database (https://talk.ictvonline.org/files/master-species-lists/), that is, ICTV Master Species List 2020.v1.xlsx. (Krupovic et al. 2020; Koonin et al. 2021).
Fig. 4.
Fig. 4.
Schematic representation of TOL highlighting key questions and approaches to further illuminate cellular evolution and its connection to viral evolution. See text for more details. Asterisks: please note that horizontal evolution has been estimated to be much more prevalent than indicated in the schematic tree.
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