Giant Viruses—Big Surprises

Viruses are the most prevalent infectious agents, populating almost every ecosystem on earth. Most viruses carry only a handful of genes supporting their replication and the production of capsids. It came as a great surprise in 2003 when the first giant virus was discovered and found to have a >1 Mbp genome encoding almost a thousand proteins. Following this first discovery, dozens of giant virus strains across several viral families have been reported. Here, we provide an updated quantitative and qualitative view on giant viruses and elaborate on their shared and variable features. We review the complexity of giant viral proteomes, which include functions traditionally associated only with cellular organisms. These unprecedented functions include components of the translation machinery, DNA maintenance, and metabolic enzymes. We discuss the possible underlying evolutionary processes and mechanisms that might have shaped the diversity of giant viruses and their genomes, highlighting their remarkable capacity to hijack genes and genomic sequences from their hosts and environments. This leads us to examine prominent theories regarding the origin of giant viruses. Finally, we present the emerging ecological view of giant viruses, found across widespread habitats and ecological systems, with respect to the environment and human health.

[1]  C. Desnues,et al.  Discovery and Further Studies on Giant Viruses at the IHU Mediterranee Infection That Modified the Perception of the Virosphere , 2019, Viruses.

[2]  K. Moelling,et al.  Viruses and Evolution – Viruses First? A Personal Perspective , 2019, Front. Microbiol..

[3]  T. Sicheritz-Pontén,et al.  Genomic and metagenomic signatures of giant viruses are ubiquitous in water samples from sewage, inland lake, waste water treatment plant, and municipal water supply in Mumbai, India , 2019, Scientific Reports.

[4]  H. Ogata,et al.  Medusavirus, a Novel Large DNA Virus Discovered from Hot Spring Water , 2019, Journal of Virology.

[5]  Thijs J. G. Ettema,et al.  Virus Genomes from Deep Sea Sediments Expand the Ocean Megavirome and Support Independent Origins of Viral Gigantism , 2018, mBio.

[6]  E. Koonin,et al.  Evolution of the Large Nucleocytoplasmic DNA Viruses of Eukaryotes and Convergent Origins of Viral Gigantism. , 2019, Advances in virus research.

[7]  D. Raoult,et al.  Ancestrality and Mosaicism of Giant Viruses Supporting the Definition of the Fourth TRUC of Microbes , 2018, Front. Microbiol..

[8]  E. Koonin,et al.  Multiple evolutionary origins of giant viruses , 2018, F1000Research.

[9]  J. Blanchard,et al.  Hidden diversity of soil giant viruses , 2018, Nature Communications.

[10]  J. Claverie,et al.  Mimiviridae: An Expanding Family of Highly Diverse Large dsDNA Viruses Infecting a Wide Phylogenetic Range of Aquatic Eukaryotes , 2018, Viruses.

[11]  J. Matsuo,et al.  Lateral Gene Transfer Between Protozoa-Related Giant Viruses of Family Mimiviridae and Chlamydiae , 2018, Evolutionary bioinformatics online.

[12]  S. Barik A Family of Novel Cyclophilins, Conserved in the Mimivirus Genus of the Giant DNA Viruses , 2018, Computational and structural biotechnology journal.

[13]  Yuquan Wei,et al.  Structural and Mechanistic Analyses Reveal a Unique Cas4-like Protein in the Mimivirus Virophage Resistance Element System , 2018, iScience.

[14]  D. Raoult,et al.  Deciphering viral presences: two novel partial giant viruses detected in marine metagenome and in a mine drainage metagenome , 2018, Virology Journal.

[15]  C. Suttle,et al.  The kinetoplastid-infecting Bodo saltans virus (BsV), a window into the most abundant giant viruses in the sea , 2017, bioRxiv.

[16]  E. Kroon,et al.  Cedratvirus getuliensis replication cycle: an in-depth morphological analysis , 2018, Scientific Reports.

[17]  G. Kroemer,et al.  Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere , 2018, Nature Communications.

[18]  E. Kroon,et al.  Ubiquitous giants: a plethora of giant viruses found in Brazil and Antarctica , 2018, Virology Journal.

[19]  Janis Kruse,et al.  Amoebae, Giant Viruses, and Virophages Make Up a Complex, Multilayered Threesome , 2018, Front. Cell. Infect. Microbiol..

[20]  Kiran Kondabagil,et al.  The number of genes encoding repeat domain-containing proteins positively correlates with genome size in amoebal giant viruses , 2018, Virus evolution.

[21]  Elliot J. Lefkowitz,et al.  Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV) , 2017, Nucleic Acids Res..

[22]  D. Raoult,et al.  Giant Viruses of Amoebae: A Journey Through Innovative Research and Paradigm Changes. , 2017, Annual review of virology.

[23]  P. Forterre Viruses in the 21st Century: From the Curiosity-Driven Discovery of Giant Viruses to New Concepts and Definition of Life. , 2017, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[24]  E. Koonin,et al.  Polintons, virophages and transpovirons: a tangled web linking viruses, transposons and immunity. , 2017, Current opinion in virology.

[25]  A. Katzourakis,et al.  Disentangling the origins of virophages and polintons. , 2017, Current opinion in virology.

[26]  J. Claverie,et al.  Comparative Genomics of Chrysochromulina Ericina Virus and Other Microalga-Infecting Large DNA Viruses Highlights Their Intricate Evolutionary Relationship with the Established Mimiviridae Family , 2017, Journal of Virology.

[27]  Natalia N. Ivanova,et al.  Giant viruses with an expanded complement of translation system components , 2017, Science.

[28]  M. Middelboe,et al.  A Student’s Guide to Giant Viruses Infecting Small Eukaryotes: From Acanthamoeba to Zooxanthellae , 2017, Viruses.

[29]  D. Raoult,et al.  Mimivirus: leading the way in the discovery of giant viruses of amoebae , 2017, Nature Reviews Microbiology.

[30]  B. La Scola,et al.  The analysis of translation-related gene set boosts debates around origin and evolution of mimiviruses , 2017, PLoS genetics.

[31]  Lubos Klucar,et al.  viruSITE—integrated database for viral genomics , 2016, Database J. Biol. Databases Curation.

[32]  T. Hackl,et al.  Host genome integration and giant virus-induced reactivation of the virophage mavirus , 2016, Nature.

[33]  F. Maruyama,et al.  Evolution and Phylogeny of Large DNA Viruses, Mimiviridae and Phycodnaviridae Including Newly Characterized Heterosigma akashiwo Virus , 2016, Front. Microbiol..

[34]  D. Raoult,et al.  Cedratvirus, a Double-Cork Structured Giant Virus, is a Distant Relative of Pithoviruses , 2016, Viruses.

[35]  Philippe Colson,et al.  The Expanding Family of Virophages , 2016, Viruses.

[36]  M. Moniruzzaman,et al.  Standing on the Shoulders of Giant Viruses: Five Lessons Learned about Large Viruses Infecting Small Eukaryotes and the Opportunities They Create , 2016, PLoS pathogens.

[37]  D. Raoult,et al.  Mimivirus inaugurated in the 21st century the beginning of a reclassification of viruses. , 2016, Current opinion in microbiology.

[38]  E. Kroon,et al.  Giants among larges: how gigantism impacts giant virus entry into amoebae. , 2016, Current opinion in microbiology.

[39]  M. Linial,et al.  Gene overlapping and size constraints in the viral world , 2016, Biology Direct.

[40]  Philippe Colson,et al.  Giant Viruses of Amoebas: An Update , 2016, Front. Microbiol..

[41]  Didier Raoult,et al.  MIMIVIRE is a defence system in mimivirus that confers resistance to virophage , 2016, Nature.

[42]  B. La Scola,et al.  A Brazilian Marseillevirus Is the Founding Member of a Lineage in Family Marseilleviridae , 2016, Viruses.

[43]  J. Claverie,et al.  The rapidly expanding universe of giant viruses: Mimivirus, Pandoravirus, Pithovirus and Mollivirus. , 2015, FEMS microbiology reviews.

[44]  A. Gasbarrini,et al.  The human gut microbiota and virome: Potential therapeutic implications , 2015, Digestive and Liver Disease.

[45]  Markus H. Antwerpen,et al.  Whole-Genome Sequencing of a Pandoravirus Isolated from Keratitis-Inducing Acanthamoeba , 2015, Genome Announcements.

[46]  M. Pérez‐Losada,et al.  Recombination in viruses: Mechanisms, methods of study, and evolutionary consequences , 2014, Infection, Genetics and Evolution.

[47]  J. Claverie,et al.  From extraordinary endocytobionts to Pandoraviruses. Comment on Scheid et al.: Some secrets are revealed: Parasitic keratitis amoebae as vectors of the scarcely described pandoraviruses to humans , 2015, Parasitology Research.

[48]  E. Koonin,et al.  Origin of giant viruses from smaller DNA viruses not from a fourth domain of cellular life. , 2014, Virology.

[49]  B. La Scola,et al.  Acanthamoeba polyphaga mimivirus and other giant viruses: an open field to outstanding discoveries , 2014, Virology Journal.

[50]  C. Robert,et al.  Samba virus: a novel mimivirus from a giant rain forest, the Brazilian Amazon , 2014, Virology Journal.

[51]  J. Claverie,et al.  Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology , 2014, Proceedings of the National Academy of Sciences.

[52]  B. La Scola,et al.  A resourceful giant: APMV is able to interfere with the human type I interferon system. , 2014, Microbes and infection.

[53]  C. Robert,et al.  Complete genome sequence of Courdo11 virus, a member of the family Mimiviridae , 2013, Virus Genes.

[54]  C. Desnues,et al.  Describing the Silent Human Virome with an Emphasis on Giant Viruses , 2013, Intervirology.

[55]  Jean-Michel Claverie,et al.  Pandoraviruses: Amoeba Viruses with Genomes Up to 2.5 Mb Reaching That of Parasitic Eukaryotes , 2013, Science.

[56]  C. Desnues,et al.  Evidence of the megavirome in humans. , 2013, Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology.

[57]  E. Koonin,et al.  Mimiviridae: clusters of orthologous genes, reconstruction of gene repertoire evolution and proposed expansion of the giant virus family , 2013, Virology Journal.

[58]  Eugene V. Koonin,et al.  Provirophages and transpovirons as the diverse mobilome of giant viruses , 2012, Proceedings of the National Academy of Sciences.

[59]  A. Nasir,et al.  Giant viruses coexisted with the cellular ancestors and represent a distinct supergroup along with superkingdoms Archaea, Bacteria and Eukarya , 2012, BMC Evolutionary Biology.

[60]  M. Fischer Sputnik and Mavirus: more than just satellite viruses , 2011, Nature Reviews Microbiology.

[61]  Elliot J. Lefkowitz,et al.  Virus taxonomy: classification and nomenclature of viruses , 2012 .

[62]  J. Claverie,et al.  Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae , 2011, Proceedings of the National Academy of Sciences.

[63]  E. Holmes What Does Virus Evolution Tell Us about Virus Origins? , 2011, Journal of Virology.

[64]  J. Claverie,et al.  Breaking the 1000-gene barrier for Mimivirus using ultra-deep genome and transcriptome sequencing , 2011, Virology Journal.

[65]  C. Suttle,et al.  Giant virus with a remarkable complement of genes infects marine zooplankton , 2010, Proceedings of the National Academy of Sciences.

[66]  Michael Chandler,et al.  Gene Exchange and the Origin of Giant Viruses , 2010, Intervirology.

[67]  E. Koonin,et al.  Origin and Evolution of Eukaryotic Large Nucleo-Cytoplasmic DNA Viruses , 2010, Intervirology.

[68]  Eugene V. Koonin,et al.  Giant Marseillevirus highlights the role of amoebae as a melting pot in emergence of chimeric microorganisms , 2009, Proceedings of the National Academy of Sciences.

[69]  E. Koonin,et al.  Evolution of DNA ligases of Nucleo-Cytoplasmic Large DNA viruses of eukaryotes: a case of hidden complexity , 2009, Biology Direct.

[70]  Natalya Yutin,et al.  Eukaryotic large nucleo-cytoplasmic DNA viruses: Clusters of orthologous genes and reconstruction of viral genome evolution , 2009, Virology Journal.

[71]  Michal Linial,et al.  Viral adaptation to host: a proteome-based analysis of codon usage and amino acid preferences , 2009, Molecular systems biology.

[72]  H. Brüssow The not so universal tree of life or the place of viruses in the living world , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[73]  Andrew Rambaut,et al.  Evolutionary analysis of the dynamics of viral infectious disease , 2009, Nature Reviews Genetics.

[74]  D. Moreira,et al.  Ten reasons to exclude viruses from the tree of life , 2009, Nature Reviews Microbiology.

[75]  Didier Raoult,et al.  The virophage as a unique parasite of the giant mimivirus , 2008, Nature.

[76]  P. Forterre,et al.  Redefining viruses: lessons from Mimivirus , 2008, Nature Reviews Microbiology.

[77]  D. Moreira,et al.  Giant viruses, giant chimeras: The multiple evolutionary histories of Mimivirus genes , 2008, BMC Evolutionary Biology.

[78]  C. Suttle Marine viruses — major players in the global ecosystem , 2007, Nature Reviews Microbiology.

[79]  D. Raoult,et al.  Ultrastructural Characterization of the Giant Volcano-like Virus Factory of Acanthamoeba polyphaga Mimivirus , 2007, PloS one.

[80]  Patrick Forterre,et al.  The origin of viruses and their possible roles in major evolutionary transitions. , 2006, Virus research.

[81]  Eugene V Koonin,et al.  Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. , 2006, Virus research.

[82]  D. Stuart,et al.  What does structure tell us about virus evolution? , 2005, Current opinion in structural biology.

[83]  Chuan Xiao,et al.  Cryo-electron microscopy of the giant Mimivirus. , 2005, Journal of molecular biology.

[84]  J. Claverie,et al.  The 1.2-Megabase Genome Sequence of Mimivirus , 2004, Science.

[85]  J. V. Etten,et al.  Unusual Life Style of Giant Chlorella Viruses , 2003 .

[86]  Jean-Michel Claverie,et al.  A Giant Virus in Amoebae , 2003, Science.

[87]  E. Koonin,et al.  Common Origin of Four Diverse Families of Large Eukaryotic DNA Viruses , 2001, Journal of Virology.

[88]  J. V. Van Etten,et al.  Giant viruses infecting algae. , 1999, Annual review of microbiology.

[89]  S. Elena,et al.  Basic concepts in RNA virus evolution , 1996, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.