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The LUCA and Its Complex Virome in Another Recent Synthesis, We Examined the Origins of the Replication and Structural Mart Krupovic , Valerian V

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The LUCA and Its Complex Virome in Another Recent Synthesis, We Examined the Origins of the Replication and Structural Mart Krupovic , Valerian V PERSPECTIVES archaea that form several distinct, seemingly unrelated groups16–18. The LUCA and its complex virome In another recent synthesis, we examined the origins of the replication and structural Mart Krupovic , Valerian V. Dolja and Eugene V. Koonin modules of viruses and posited a ‘chimeric’ scenario of virus evolution19. Under this Abstract | The last universal cellular ancestor (LUCA) is the most recent population model, the replication machineries of each of of organisms from which all cellular life on Earth descends. The reconstruction of the four realms derive from the primordial the genome and phenotype of the LUCA is a major challenge in evolutionary pool of genetic elements, whereas the major biology. Given that all life forms are associated with viruses and/or other mobile virion structural proteins were acquired genetic elements, there is no doubt that the LUCA was a host to viruses. Here, by from cellular hosts at different stages of evolution giving rise to bona fide viruses. projecting back in time using the extant distribution of viruses across the two In this Perspective article, we combine primary domains of life, bacteria and archaea, and tracing the evolutionary this recent work with observations on the histories of some key virus genes, we attempt a reconstruction of the LUCA virome. host ranges of viruses in each of the four Even a conservative version of this reconstruction suggests a remarkably complex realms, along with deeper reconstructions virome that already included the main groups of extant viruses of bacteria and of virus evolution, to tentatively infer archaea. We further present evidence of extensive virus evolution antedating the the composition of the virome of the last universal cellular ancestor (LUCA; also LUCA. The presence of a highly complex virome implies the substantial genomic referred to as the last universal common and pan-genomic complexity of the LUCA itself. ancestor of cellular organisms). Viruses and other mobile genetic elements transcriptases (RTs). Monodnaviria includes The LUCA (MGEs) are involved in parasitic or single- stranded DNA (ssDNA) viruses Evidently, to make any meaningful symbiotic relationships with all cellular together with small double-stranded DNA inferences regarding the viruses that life forms1–5, and theoretical models (dsDNA) viruses (papillomaviruses and infected the LUCA, we must have at least indicate that the emergence of such selfish polyomaviruses) that are unified by the a general notion of the characteristics elements is an intrinsic feature of replicator distinct endonuclease (or its inactivated of this ancestral life form. Considerable systems6–11. Thus, genetic parasites must derivative) involved in the initiation efforts have been undertaken over the have been inalienable components of life of genome replication. Duplodnaviria years to deduce the genetic composition from its very beginnings. Unlike cellular include tailed dsDNA bacteriophages and biological features of the LUCA from life forms, viruses employ all existing types and archaeal viruses along with animal comparative genome analyses combined of nucleic acids as replicating genomes herpesviruses that are unified by the with biological reasoning20–22. These packaged into virions. This diversity of distinct morphogenetic module consisting inferences are challenged by the complex the replication and expression strategies of HK97- fold major capsid proteins evolutionary histories of most genes (with has been captured in a systematic form in (MCPs), homologous genome packaging partial exception for the core components the ‘Baltimore classification’ of viruses12. ATPases- nucleases (terminases), portal of the translation and transcription systems) Recently, we undertook a comprehensive proteins and capsid maturation proteases. that involved extensive horizontal transfer reappraisal of the findings of virus Varidnaviria is an enormously diverse and non- orthologous gene displacement23–25. phylogenomics to assess the evolutionary assemblage of viruses infecting bacteria, Nevertheless, on the strength of combined status of each of the Baltimore classification archaea and eukaryotes that are unified by evidence, it appears likely that the LUCA groups13. This synthesis culminated in the the vertical jelly-roll MCPs (most groups was a prokaryote-like organism (that is, like identification of four realms (the highest possess double jelly-roll (DJR) MCPs but bacteria or archaea) of considerable genomic rank in virus taxonomy) of viruses that are some have a single jelly-roll (SJR) domain and organizational complexity20,26–28. Formal monophyletic with respect to their core gene that is the likely ancestral form) along reconstructions of the ancestral gene sets and partially overlap with the Baltimore with a distinct type of genome packaging repertoires based on maximum parsimony classification: Riboviria, Monodnaviria, ATPase present in most constituent and maximum likelihood approaches Duplodnaviria and Varidnaviria. Riboviria groups. This megataxonomy of viruses assign several hundred genes to the LUCA includes viruses with positive- sense, has been recently formally adopted by the that are responsible for most of the core negative- sense and double- stranded International Committee for the Taxonomy processes characteristic of prokaryotic RNA (dsRNA) genomes as well as of Viruses14,15. Apart from the four cells22,27,29, perhaps making it comparable to reverse- transcribing viruses with RNA and monophyletic realms, several groups of the simplest extant free- living bacteria and DNA genomes. Members of this realm are viruses remain unaffiliated in the emergent archaea (~1,000 genes or even more complex unified by the homologous RNA-dependent megataxonomy, most notably the diverse given that the accessory gene repertoire RNA polymerases (RdRPs) and reverse dsDNA viruses of hyperthermophilic is not amenable to a straightforward NATURE REVIEWS | MICROBIOLOGY PERSPECTIVES reconstruction). However, the nature of the with the results of recent experiments to the LUCA virome, indicating that replication and membrane machineries of demonstrating the viability of bacteria with (at least) this realm of viruses had already LUCA remains unclear owing to the drastic an engineered, mixed archaeal–bacterial reached considerable diversity prior to the differences between the respective systems membrane44. The same considerations apply radiation of archaea and bacteria (Fig. 3). of bacteria and archaea, the two primary to the cell wall, which is represented by the All viruses of this realm share homologous domains of life30–33. peptidoglycan in most bacteria45,46 and MCPs (HK97- fold), large and small The fact that the replicative DNA the proteinaceous S-layer in archaea terminase subunits, prohead maturation polymerases of bacteria, archaea and and some bacteria47. Importantly, however, proteases and portal proteins, indicating eukaryotes are not homologous has in this case, the possibility of a wall-less that their morphogenetic modules are prompted ideas of an RNA-based LUCA cannot be dismissed. monophyletic53–58. Duplodnaviruses are LUCA31,34,35. However, the recent discovery The genetic composition of modern broadly distributed among both bacteria and of the structural similarity between the prokaryotes is best described in terms of archaea (Figs 1,2) and, crucially, comparative catalytic cores of the archaeal replicative the pangenome, that is, the entirety of the genomic analyses suggest that the archaeal family D DNA polymerase (PolD) genes that are found in organisms with and bacterial viruses within Duplodnaviria, and the universal DNA-directed RNA closely related core genomes that are on a broad scale, have coevolved with their polymerase36,37 implies a common origin traditionally considered to constitute a respective hosts59 (see discussion below). of replication and transcription and species48–50. The accessory genes that are Tailed bacteriophages are nearly suggests an ‘archaeal-like’ replication present in each strain in addition to the universal among bacteria60. In archaea, machinery in LUCA, with PolD serving core genome and collectively account duplodnaviruses or related proviruses as the replicative DNA polymerases38. for the bulk of the pangenome include (virus genome integrated into the cellular Evolutionary reconstructions point to a diverse anti- parasite defence systems, genes chromosome) have been detected in fairly complex replication apparatus in the involved in inter-microbial conflicts, such many mesophilic as well as extremophilic LUCA, with processive replication aided as antibiotic production and resistance, lineages of the phyla Euryarchaeota by the sliding clamp (proliferating cell and integrated MGEs. Given that genetic and Thaumarchaeota56,61. Furthermore, nuclear antigen), clamp loader, replicative parasites are intrinsic components of any HK97- fold MCPs were identified in helicase and the ssDNA-binding protein. replicator system, this pangenome structure uncultivated archaea of the proposed Similarly, the transcription system of the should necessarily have been established at phyla Aenigmarchaeota, Altiarchaeota, LUCA can be inferred to have already the earliest stages of cellular evolution. Thus, Nanoarchaeota, Micrarchaeota, included a multisubunit RNA polymerase although important features of the LUCA Iainarchaeota and Asgardarchaeota (Fig. 2). with the duplicated large subunits, some remain to be clarified, we can conclude However, given the potential artefacts
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