Giant DNA viruses make big strides in eukaryote evolution

Nucleocytoplasmic large DNA viruses (NCLDVs) are widespread in the biosphere. This issue of Cell Host & Microbe, Nelson et al., and a recent Nature paper, Moniruzzaman show NCLDVs can integrate into host genomes, highlighting mechanism large-scale virus-mediated horizontal gene transfer (vHGT) driving eukaryotic evolution. “The Modern Synthesis” evolutionary theory, formulated mid-20th century, posited that genetic mutations (along with sexual recombination) primary sources novelty These variations transferred from parents to offspring during reproduction by vertical (VGT) provide raw materials for natural selection. With rediscovery endosymbiosis theory Lynn Margulis 1970, it has been widely recognized novel genes also originate symbiotic uptake foreign cell another cell, subsequent integration endosymbiont massive nuclear genome host. The transmission between different genomes is known as (HGT), when intracellular symbionts involved, endosymbiotic (eHGT) (Figure 1A). era genomics-based sequence analyses 21st century led discovery numerous variation (Shapiro, 2016Shapiro J.A. Nothing Evolution Makes Sense Except Light Genomics: Read-Write Genome an Active Biological Process.Biology (Basel). 2016; 5: 27Google Scholar), among them HGT-mediated viruses, here termed viral (vHGT). Small endogenous elements (EVEs), integrated genome, particular retroviruses (ERVs), have received most attention given ~10% mammalian consists ERVs. 2003 first giant double-stranded virus, Acanthameba polyphaga mimivirus (APMV), heralded advent “new microbiology” (Fischer, 2016Fischer M.G. Giant come age.Curr. Opin. Microbiol. 31: 50-57Crossref Scopus (36) Google Scholar). Its ~1.2 Mbp encodes almost one thousand unprecedented functions such components translation system, repair, metabolic enzymes. Since their discovery, nucleocytoplasmic (NCLDVs), found be abundant biosphere, especially aquatic systems (Brandes Linial, 2019Brandes N. Linial M. viruses-big surprises.Viruses. 2019; 11: 404Crossref (22) frequently metagenomics datasets (Moniruzzaman 2020aMoniruzzaman Martinez-Gutierrez C.A. Weinheimer A.R. Aylward F.O. Dynamic evolution complex virocell metabolism globally-distributed viruses.Nat. Commun. 2020; 1710Crossref PubMed (38) global metagenomic data mining recovered 2,074 putative NCLDV populations (Schulz 2020Schulz F. Roux S. Paez-Espino D. Jungbluth Walsh D.A. Denef V.J. McMahon K.D. Konstantinidis K.T. Eloe-Fadrosh E.A. Kyrpides N.C. Woyke T. virus diversity interactions through metagenomics.Nature. 578: 432-436Crossref (67) infect wide range eukaryotes protists multicellular animals plants. Their chimeric, harboring span whole cellular life (Archaea, Bacteria, Eukarya) include homologs other groups viruses. discovered until now encode proteins roles photosynthesis, translation, transport processes, cytoskeleton, intermediary metabolism, suggesting reprogramming important strategy enhance propagation. Viral might confer transient competitive advantage infected cells, under stress conditions. Genomes grown size facilitate hosts endocytotic processes require critical minimum particle sizes. Two new studies shown NCLDVs, like some thus representing vHGT 2020bMoniruzzaman Widespread endogenization shapes green algae.Nature. 588: 141-145Crossref (24) Scholar; 2020Nelson D.R. Hazzouri K.M. Lauersen K.J. Jaiswal A. Chaiboonchoe Mystikou Fu W. Daakour Dohai B. Alzahmi al.Large-scale sequencing reveals forces microalgal evolution.Cell Microbe. 29 (this issue): 250-266Google Scholar) 1B). In this issue, Scholar identified underexplored reservoir families (VFAMs) genomes. authors completed rich repository sequences, including 107 species sampled 11 phyla indigenous varied geographies climates. Surprisingly, 91,757 domain-containing sequences were detected overall 184 algal (including newly sequenced database entries), which functionally expressed lineage-specific. family domains against coding Hidden Markov Model (HMM)-based search, proven effective retrieval elements, mostly small fragments. Many virus-derived conferred niche-specific fitness benefit host, conclude. striking example acquisition membrane transporters topology-altering proteins), hallmark distinguishing saltwater freshwater microalgae. general, marine contained significantly more than species, although terrestrial not discriminated, negatively affected count species. Chlorovirus, Coccolithovirus, Pandoravirus, Marseillevirus, Tupanvirus, others. Some algae acquired distant, unrelated clades employing broad-host shuttle vectors (Figures 1C 1D). hypothesized acquire similar result competition shared niches nutrient-limited open ocean. A related report published recently Scholar, performed analysis implementing algorithm “ViralRecall” multi-step pipeline, surveying 65 6 chlorophyte classes retrieved publicly available database. Multiple metrics used identify genomic loci. ten genes, enrichment proteins, homology nucleotide composition. signatures (“endogenization”) 24 analyzed (GEVEs) ranged 78 1,925 kb, 1,782 predicted comprised many 10% total reading frames (e.g., Tetrabaena socialis). GEVEs derived two families, Phycodnaviridae Mimiviridae. Interestingly, several surveyed GEVE, independent events, cases involving families. Several 12 additional even though could recovered, decay fragmentation. presence spliceosomal introns all confirmed Segmental duplications losses, e.g., indicated rearrangements after integration. addition GEVEs, encoded best matches analyzed, strongly rather rule exception algae. studies, processing, both demonstrated prevalence NCLDV-derived underappreciated aspect vHGT. shed light on controversial namely extent significance non-endosymbiotic HGT eukaryotes. Whereas pervasive continuous prokaryotes, generating pangenomes, often thought episodic, contributing long-term content (Ku 2015Ku C. Nelson-Sathi Roettger Sousa F.L. Lockhart P.J. Bryant Hazkani-Covo E. McInerney J.O. Landan G. Martin W.F. Endosymbiotic origin differential loss genes.Nature. 2015; 524: 427-432Crossref (169) growing number bacterial alien then either interpreted caused contaminations or progenitors plastids mitochondria coupled losses lineages. mediated challenge view because they plausible eukaryote transfers occur archaeal vHGT, cannot directly prokaryotes. It prokaryotic infection cycle bacteria phagocytosed food vacuoles reside cytoplasm 1C). exploding universe role shaping exciting avenues further research. remains shown, example, how impinge phenotype, whether generate taxa (of ranks), long what incongruences phylogenetic trees explained sampling vHGTs. development single-cell genomics projects (such TARA Oceans Project, Earth Microbiome Ecobiomics etc.), biosphere will unfold “iceberg” gradually emerge. All these enable researchers better understand evolution, practical perspective, predict outbreak next pandemics. work was supported following funding S.C. at Agricultural Genomics Institute Shenzhen (AGIS), Chinese Academy Sciences (CAAS): Science Technology Innovation Program (ASTIP), Guangdong technology foundation (2019ZT08N628), National Natural Foundation China ( 32022006 ). Large-scale evolutionNelson al.Cell MicrobeJanuary 11, 2021In BriefNelson al. combine high-throughput cultivation, sequencing, bioinformatics strategies resources gaining perspectives microalgae diverse lineages environments. resource greatly expands collection provides insight shaped major clades. Full-Text PDF