Nucleocytoplasmic large DNA viruses (NCLDVs) are a group of large viruses that infect a wide range of hosts, from animals to protists. These viruses are grouped together in NCLDV based on genomic sequence analyses. They share a set of essential genes for virion morphogenesis and replication. Most NCLDVs generally have large physical sizes while their morphologies vary in different families, such as icosahedral, brick, or oval shape, raising the question of the possible regulatory factor on their morphogenesis. The capsids of icosahedral NCLDVs are assembled from small building blocks, named capsomers, which are the trimeric form of the major capsid proteins. Note that the capsids of immature poxvirus are spherical even though they are assembled from capsomers that share high structural conservation with those icosahedral NCLDVs. The recently published high resolution structure of NCLDVs, Paramecium bursaria Chlorella virus 1 and African swine fever virus, described the intensive network of minor capsid proteins that are located underneath the capsomers. Among these minor proteins is the elongated tape measure protein (TmP) that spans from one icosahedral fivefold vertex to another. In this study, we focused on the critical roles that TmP plays in the assembly of icosahedral NCLDV capsids, answering a question raised in a previously proposed spiral mechanism. Interestingly, basic local alignment search on the TmPs showed no significant hits in poxviruses, which might be the factor that differentiates poxviruses and icosahedral NCLDVs in their morphogenesis.
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References
1.
AbrahaoJ, SilvaL, SilvaLS, et al.Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere. Nat Commun, 2018; 9:749.
2.
AbrahaoJS, AraujoR, ColsonP, et al.The analysis of translation-related gene set boosts debates around origin and evolution of mimiviruses. PLoS Genet, 2017; 13:e1006532.
3.
AlonsoC, BorcaM, DixonL, et al.ICTV virus taxonomy profile: Asfarviridae. J Gen Virol, 2018; 99:613–614.
4.
AltschulSF, GishW, MillerW, et al.Basic local alignment search tool. J Mol Biol, 1990; 215:403–410.
5.
AsgariS, BideshiDK, BigotY, et al.ICTV virus taxonomy profile: Ascoviridae. J Gen Virol, 2017; 98:4–5.
6.
BaharMW, GrahamSC, StuartDI, et al.Insights into the evolution of a complex virus from the crystal structure of Vaccinia virus D13. Structure, 2011; 19:1011–1020.
7.
BensonSD, BamfordJK, BamfordDH, et al.Does common architecture reveal a viral lineage spanning all three domains of life?. Mol Cell, 2004; 16:673–685.
8.
BoyerM, YutinN, PagnierI, et al.Giant Marseillevirus highlights the role of Amoebae as a melting pot in emergence of chimeric microorganisms. Proc Natl Acad Sci U S A, 2009; 106:21848–21853.
9.
BrandesN, and LinialM. Giant viruses-big surprises. Viruses, 2019; 11:404.
10.
CamposRK, BorattoPV, AssisFL, et al.Samba virus: a novel Mimivirus from a giant rain forest, the Brazilian Amazon. Virol J, 2014; 11:95.
11.
CasparDL, and KlugA. Physical principles in the construction of regular viruses. Cold Spring Harb Symp Quant Biol, 1962; 27:1–24.
12.
CherrierMV, KostyuchenkoVA, XiaoC, et al.An icosahedral algal virus has a complex unique vertex decorated by a spike. Proc Natl Acad Sci U S A, 2009; 106:11085–11089.
13.
ChichonFJ, RodriguezMJ, RiscoC, et al.Membrane remodelling during Vaccinia virus morphogenesis. Biol Cell, 2009; 101:401–414.
14.
ChincharVG, HickP, InceIA, et al.ICTV virus taxonomy profile: Iridoviridae. J Gen Virol, 2017; 98:890–891.
15.
ChlandaP, CarbajalMA, CyrklaffM, et al.Membrane rupture generates single open membrane sheets during Vaccinia virus assembly. Cell Host Microbe, 2009; 6:81–90.
16.
ClaverieJM, and AbergelC. Mimivirus and its virophage. Annu Rev Genet, 2009; 43:49–66.
17.
ClaverieJM, AbergelC, and OgataH. Mimivirus. Curr Top Microbiol Immunol, 2009; 328:89–121.
18.
ClaverieJM, OgataH, AudicS, et al.Mimivirus and the emerging concept of “giant” virus. Virus Res, 2006; 117:133–144.
19.
ColsonP, de LamballerieX, FournousG, et al.Reclassification of giant viruses composing a fourth domain of life in the new order Megavirales. Intervirology, 2012; 55:321–332.
20.
FangQ, ZhuD, AgarkovaI, et al.Near-atomic structure of a giant virus. Nat Commun, 2019; 10:388.
21.
FileeJ. Lateral gene transfer, lineage-specific gene expansion and the evolution of nucleo cytoplasmic large DNA viruses. J Invertebr Pathol, 2009; 101:169–171.
22.
GanserBK, LiS, KlishkoVY, et al.Assembly and analysis of conical models for the HIV-1 core. Science, 1999; 283:80–83.
23.
HughesAL, IrausquinS, and FriedmanR. The evolutionary biology of poxviruses. Infect Genet Evol, 2010; 10:50–59.
24.
IyerLM, AravindL, and KooninEV. Common origin of four diverse families of large eukaryotic DNA viruses. J Virol, 2001; 75:11720–11734.
25.
KloseT, KuznetsovYG, XiaoC, et al.The three-dimensional structure of Mimivirus. Intervirology, 2010; 53:268–273.
26.
KloseT, RetenoDG, BenamarS, et al.Structure of Faustovirus, a large dsDNA virus. Proc Natl Acad Sci U S A, 2016; 113:6206–6211.
27.
KooninEV, KrupovicM, and YutinN. Evolution of double-stranded DNA viruses of eukaryotes: from bacteriophages to transposons to giant viruses. Ann N Y Acad Sci, 2015; 1341:10–24.
28.
KooninEV, and YutinN. Multiple evolutionary origins of giant viruses. F1000Res, 2018; 7:F1000 Faculty Rev-1840.
29.
Krijnse LockerJ, ChlandaP, SachsenheimerT, et al.Poxvirus membrane biogenesis: rupture not disruption. Cell Microbiol, 2013; 15:190–199.
30.
La ScolaB, AudicS, RobertC, et al.A giant virus in Amoebae. Science, 2003; 299:2033.
31.
LegendreM, BartoliJ, ShmakovaL, et al.Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a Pandoravirus morphology. Proc Natl Acad Sci U S A, 2014; 111:4274–4279.
32.
LetunicI.PhyloT v2: a phylogenetic tree generator, based on NCBI or GTD taxonomy. https://phylot.biobyte.de/ (Last accessed on March4, 2020).
33.
LetunicI, and BorkP. Interactive tree of life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics, 2007; 23:127–128.
34.
LiuL, CooperT, HowleyPM, et al.From crescent to mature virion: Vaccinia virus assembly and maturation. Viruses, 2014; 6:3787–3808.
35.
LiuS, LuoY, WangY, et al.Cryo-EM structure of the African swine fever virus. Cell Host Microbe, 2019; 26:836–843.e3.
36.
Lopez-GarciaP. The place of viruses in biology in light of the metabolism-versus-replication-first debate. Hist Philos Life Sci, 2012; 34:391–406.
37.
MilrotE, MutsafiY, Fridmann-SirkisY, et al.Virus-host interactions: insights from the replication cycle of the large Paramecium bursaria chlorella virus. Cell Microbiol, 2016; 18:3–16.
38.
MoreiraD, and Brochier-ArmanetC. Giant viruses, giant chimeras: the multiple evolutionary histories of Mimivirus genes. BMC Evol Biol, 2008; 8:12.
39.
MoreiraD, and Lopez-GarciaP. Ten reasons to exclude viruses from the tree of life. Nat Rev Microbiol, 2009; 7:306–311.
40.
MoreiraD, and Lopez-GarciaP. Evolution of viruses and cells: do we need a fourth domain of life to explain the origin of eukaryotes?. Philos Trans R Soc Lond B Biol Sci, 2015; 370:20140327.
41.
MountDW. Using the basic local alignment search tool (BLAST). CSH Protoc, 2007; 2007:pdb top17.
42.
MutsafiY, ShimoniE, ShimonA, et al.Membrane assembly during the infection cycle of the giant Mimivirus. PLoS Pathog, 2013; 9:e1003367.
43.
NandhagopalN, SimpsonAA, GurnonJR, et al.The structure and evolution of the major capsid protein of a large, lipid-containing DNA virus. Proc Natl Acad Sci U S A, 2002; 99:14758–14763.
44.
NasirA, KimKM, and Caetano-AnollesG. Phylogenetic tracings of proteome size support the gradual accretion of protein structural domains and the early origin of viruses from primordial cells. Front Microbiol, 2017; 8:1178.
45.
PhilippeN, LegendreM, DoutreG, et al.Pandoraviruses: Amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science, 2013; 341:281–286.
46.
RaoultD. There is no such thing as a tree of life (and of course viruses are out!). Nat Rev Microbiol, 2009; 7:615; author reply 615.
47.
RaoultD. TRUC or the need for a new microbial classification. Intervirology, 2013; 56:349–353.
48.
RossmannMG, and JohnsonJE. Icosahedral RNA virus structure. Annu Rev Biochem, 1989; 58:533–573.
49.
SinkovitsRS, and BakerTS. A tale of two symmetrons: rules for construction of icosahedral capsids from trisymmetrons and pentasymmetrons. J Struct Biol, 2010; 170:109–116.
50.
SuarezC, AndresG, KolovouA, et al.African swine fever virus assembles a single membrane derived from rupture of the endoplasmic reticulum. Cell Microbiol, 2015; 17:1683–1698.
51.
SuarezC, WelschS, ChlandaP, et al.Open membranes are the precursors for assembly of large DNA viruses. Cell Microbiol, 2013; 15:1883–1895.
52.
SubramaniamK, BehringerDC, BojkoJ, et al.A new family of DNA viruses causing disease in crustaceans from diverse aquatic biomes. mBio, 2020; 11 [Epub ahead of print]; DOI: 10.1128/mBio.02938-19.
53.
SzajnerP, WeisbergAS, LebowitzJ, et al.External scaffold of spherical immature poxvirus particles is made of protein trimers, forming a honeycomb lattice. J Cell Biol, 2005; 170:971–981.
54.
TakemuraM, YokoboriS, and OgataH. Evolution of eukaryotic DNA polymerases via interaction between cells and large DNA viruses. J Mol Evol, 2015; 81:24–33.
55.
WangN, ZhaoD, WangJ, et al.Architecture of African swine fever virus and implications for viral assembly. Science, 2019; 366:640–644.
56.
WilliamsTA, EmbleyTM, and HeinzE. Informational gene phylogenies do not support a fourth domain of life for nucleocytoplasmic large DNA viruses. PLoS One, 2011; 6:e21080.
57.
WilsonWH, Van EttenJL, and AllenMJ. The Phycodnaviridae: the story of how tiny giants rule the world. Curr Top Microbiol Immunol, 2009; 328:1–42.
58.
WrigleyNG. An electron microscope study of the structure of Sericesthis iridescent virus. J Gen Virol, 1969; 5:123–134.
59.
XianY, KarkiCB, SilvaSM, et al.The roles of electrostatic interactions in capsid assembly mechanisms of giant viruses. Int J Mol Sci, 2019; 20:1876.
60.
XiaoC, ChipmanPR, BattistiAJ, et al.Cryo-electron microscopy of the giant Mimivirus. J Mol Biol, 2005; 353:493–496.
61.
XiaoC, FischerMG, BolotauloDM, et al.Cryo-EM reconstruction of the Cafeteria roenbergensis virus capsid suggests novel assembly pathway for giant viruses. Sci Rep, 2017; 7:5484.
62.
XiaoC, FischerMG, BolotauloDM, et al. Supplementary 2. Cryo-EM reconstruction of the Cafeteria roenbergensis virus capsid suggests novel assembly pathway for giant viruses. https://static-content.springer.com/esm/art%3A10.1038%2Fs41598-017-05824-w/MediaObjects/41598_2017_5824_MOESM2_ESM.mov (Last accessed on June19, 2020).
63.
XiaoC, KuznetsovYG, SunS, et al.Structural studies of the giant Mimivirus. PLoS Biol, 2009; 7:e1000092.
64.
XiaoC, and RossmannMG. Structures of giant icosahedral eukaryotic dsDNA viruses. Curr Opin Virol, 2011; 1:101–109.
65.
YanX, ChipmanPR, CastbergT, et al.The marine algal virus PpV01 has an icosahedral capsid with T = 219 quasisymmetry. J Virol, 2005; 79:9236–9243.
66.
YanX, OlsonNH, Van EttenJL, et al.Structure and assembly of large lipid-containing dsDNA viruses. Nat Struct Biol, 2000; 7:101–103.
67.
YanX, YuZ, ZhangP, et al.The capsid proteins of a large, icosahedral dsDNA virus. J Mol Biol, 2009; 385:1287–1299.
68.
YangZ, LaskerK, Schneidman-DuhovnyD, et al.UCSF chimera, MODELLER, and IMP: an integrated modeling system. J Struct Biol, 2012; 179:269–278.
69.
YutinN, ColsonP, RaoultD, et al.Mimiviridae: clusters of orthologous genes, reconstruction of gene repertoire evolution and proposed expansion of the giant virus family. Virol J, 2013; 10:106.
70.
YutinN, and KooninEV. Hidden evolutionary complexity of nucleo-cytoplasmic large DNA viruses of eukaryotes. Virol J, 2012; 9:161.
71.
YutinN, WolfYI, and KooninEV. Origin of giant viruses from smaller DNA viruses not from a fourth domain of cellular life. Virology, 2014; 466–467:38–52.
72.
YutinN, WolfYI, RaoultD, et al.Eukaryotic large nucleo-cytoplasmic DNA viruses: clusters of orthologous genes and reconstruction of viral genome evolution. Virol J, 2009; 6:223.
73.
ZaubermanN, MutsafiY, HalevyDB, et al.Distinct DNA exit and packaging portals in the virus Acanthamoeba polyphaga Mimivirus. PLoS Biol, 2008; 6:e114.
74.
ZhangX, XiangY, DuniganDD, et al.Three-dimensional structure and function of the Paramecium bursaria chlorella virus capsid. Proc Natl Acad Sci U S A, 2011; 108:14837–14842.
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