Evolution of the Nucleo-Cytoplasmic Large DNA Viruses (NCLDV)

Evolution of the Nucleo-Cytoplasmic Large DNA Viruses (NCLDV)

Evolution of the Nucleo-Cytoplasmic
Large DNA Viruses (NCLDV)
Medium-size viral genomes (>30 kb): 10 kb
Small viral genomes (<30 kb): 1 kb
Hop stunt
viroid
0.3 kb (0)
Hepatitis Δ
1.7 kb (1)
MS2 phage 3.6 kb (4)
Hepatitis C virus 9.6 kb (10)
Citrus tristeza virus 19 kb (14)
Borna disease virus 8.9 kb (6)
Human immunodeficiency
virus 1 9.2 kb (9)
African cassava
mosaic virus 5.5 kb;
2 segments (9)
M13 phage 6.4 kb (9)
Simian virus 40
5.2 kb (7)
Sulfolobus
spindle-shaped
virus-1
15.5 kb (32)
Minute virus of
mice 5.1 kb (2)
PRD1 phage 14.9 kb (31)
φ1402 phage 24 kb (42)
Abalone shriveling
syndrome-associated
virus 35 kb (28)
Human adenovirus A
34 kb (36)
Acidianus
two-tailed
virus
63 kb (72)
Τ7 phage 40 kb (60)
Ebola virus 19 kb (9)
Influenza A virus 13.5 kb; 8 segments (11)
Porcine
circovirus-1
1.8 kb (2)
Saccharomyces
cerevisiae
virus L-A
4.6 kb (3)
Hepatitis B
virus
3.0 kb (7)
Autographa
californica nucleopolyhedrovirus
134 kb (156)
λ phage 49 kb (73)
Troll phage 59 kb (109)
Heliotis virescens
ascovirus 3E
186 kb (180)
N4 phage 70 kb (72)
Frog virus 3 106 kb (99)
Colorado tick fever virus 29.2 kb; 12 segments (13)
SPO1 phage 133 kb (204)
SARS coronavirus 30 kb (14)
Large and giant viral genomes (>300 kb): 100 kb
+RNA RT
ssDNA
Mimivirus 1,181 kb (~1000)
White spot
syndrome
virus
305 kb (~500)
+RNA
-RNA
dsRNA
dsDNA
201φ2-1 phage 317 kb (461)
Human herpesvirus 6 321 kb (192)
Cafeteria roenbergensis virus 730 kb (~550)
Paramecium bursaria Chlorella
virus 1 331 kb (802)
Marseillevirus 368 kb (457)
dsDNA RT
Protein-only capsids
Icosahedral Helical
JRC Picornavirus SF
Microviridae
Bromoviridae
Polyomaviridae
Adjoining Tymoviridae
Papillomaviridae
icosahedra
Tombusviridae
Parvoviridae
Geminiviridae Ourmiaviridae
Circoviridae
(JRC?)
Birnaviridae
Concentric icosahedra
JRC-DB Reoviridae
Adenoviridae
(JRC/non-JRC)
Other folds
Leviviridae
Picobirnaviridae
Totiviridae
Partitiviridae
Closteroviridae
Flexiviridae
Virgaviridae
Potyviridae
Inoviridae
Rudiviridae
Unknown folds
Caulimoviridae
Chrysoviridae
Complex
Spindle-shaped
Bicaudoviridae
Tailed bacteriophages
and archaeal viruses Caudovirales, GTA
Capsid-less
Viroids
Narnaviridae
Hypoviridae
Endornaviridae
Membrane-containing virions Inner membrane
Isosahedral capsid; JRC-DB
Corticoviridae, Tectiviridae
STIV
NCLDV: Outer membrane
Isosahedral Concentric icosahedra
Cystoviridae
Phycodnaviridae,
Mimiviridae
Arterivirida
Flaviviridae
Hepadnaviridae
Togaviridae
Herpesvirales
Double membrane
NCLDV
Asfaviridae
Ascoviridae
Iridoviridae
Polydnaviridae
Brick-shaped
Poxviridae
(NCLDV)
Droplet-shaped
Fuselloviridae
Guttaviridae
Bottle-shaped
Ampullaviridae
Pleomorphic virions,
thread-like nucleocapsid Mononegavirales
Orthomyxoviridae
Arenaviridae
Bunyaviridae
Coronaviridae
Ophioviridae
Roniviridae
Globuloviridae
Plasmaviridae
Irregular or cone-shaped nucleocapsid
Retroviridae
Helical nucleocapsid,
elongated virions
Lipothrixviridae
Filoviridae
Membrane-only
Pleolipoviruses
Baculoviridae
Nudivirus
Nimaviridae
A reminder: Natural history of viral genes Category 3: Viral Hallmark Genes
Shared by many diverse groups of viruses
Strong support for monophyly of all viral
members of the respective gene families
Only distant homologs in cellular organisms
Play major roles in genome replication, packaging
and assembly
Can be viewed as distinguishing characters of
the ‘virus state’
Proteins encoded by viral hallmark genes
1. Jelly-roll capsid protein
2. Superfamily 3 helicase
3. RNA-dependent RNA polymerase
and Reverse transcriptase
5. Viral archaeo-eukaryotic DNA primase
6. UL9-like superfamily 2 helicase
7. Packaging ATPase of the FtsK family
4. Rolling circle replication
initiation endonuclease
8. ATPase subunit of terminase
Koonin et al., 2006
Helicase superfamily 3 is a monophyletic viral clade within a major class of P-loop NTPases
Present in a vast
variety of viruses:
from the smallest
RNA viruses
(poliovirus) to the
largest DNA viruses
(mimivirus)
LUCA
Iyer et al. (2004) J. Struct. Biol. 146:11
Origin of the eukaryotic
viruses Nucleo-cytoplasmic large DNA viruses - NCLDV
Poxviruses
~200 kbp dsDNA
~200 genes
Phycodnaviruses
~350 kbp
~400 genes
NCLDV
phylogenomics
Number of genes
assigned to a given
ancestral form
Koonin & Yutin (2010) Intervirol. 53:284
Origins of the ancestral NCLDV genes
Breakdown of the 47 genes mapped to the ancestral NCLDV genome by likely origin
Jelly-roll capsid protein
Superfamily 3 helicase
UL9-like superfamily 2 helicase
Archaeo-eukaryotic DNA primase
Packaging ATPase of FtsK family
Transcription factors
RNA capping enzyme
Ankyrin repeats
Viral
hallmark genes
from DNA
phages
Genes from
eukaryotic
host
Two pathways of the genome complexity growth in NCLDV
Horizontal gene transfer (HGT) via
recombination with genomes of the
host, viruses, or other parasites
Lineage-specific expansion of gene
families via gene duplication events
Functions of the NCLDV gene families
Dramatic evolutionary events such as massive horizontal gene transfer
between very diverse organisms including viruses, their eukaryotic hosts,
and pathogenic bacteria have shaped the genomes of NCLDV.
Not only the gradual accumulation of the infinitesimal changes favored by
Darwin
The global ecology of NCLDV
Chlorella
Micromonas
Heterosigma
Ectocarpus
Vertebrates, Insects
Coccolythophores
Acanthamoeba
Poxviruses are among the largest known
DNA viruses with a very complex life style
~200 kbp dsDNA
~200 genes
Some researchers propose that due to their complexity
and greater autonomy, poxviruses are the descendants
of parasitic cells or even the ancestors of nucleus
Localization of RNA within
virus factories that are indeed
very complex
(Row A) HeLa cells were infected with VACV for 6 h. The
cells were then stained with acridine orange (AO) and
viewed by confocal microscopy to visualize DNA (green)
and RNA (red). One entire cell (center) and the cytoplasm
of a second cell (bottom) are seen. The green stain
outside the cell is due to AO bound to the cover slip. N,
nucleus; C, cytoplasm; F, viral factory. (Row B)
Uninfected HeLa cells were transfected with anti-sense
G8R RNA labeled with digoxigenin UTP. After 6 h, the cells
were stained with sheep anti-digoxigenin-fluorescein,
followed by Alexa Fluor 488 donkey anti-sheep (green)
and DAPI (blue). (Row C) HeLa cells were infected with
VACV and transfected 1 h later with anti-sense G8R RNA
labeled with digoxigenin UTP. (Row D) Uninfected HeLa
cells were transfected with biotinylated poly (U). After 6 h,
the cells were stained with streptavidin Alexa Fluor 488,
followed by anti-Alexa Fluor 488 rabbit IgG (green) and
DAPI (blue). (Row E) HeLa cells were infected with VACV
and transfected 1 h later with biotinylated poly (U) and
processed as in Row D.
Protein synthesis within virus factories
(Rows A, B) HeLa cells were infected with 1 PFU per cell of VACV expressing β–Galactosidase. After 6 h the
cells were stained with rabbit β–Galactosidase antibody (green), followed by Alexa Fluor 488 goat anti-rabbit
IgG and DAPI. In row B, the nuclei and factories are in 3 separate cells. (Rows C–F) Hela cells were infected
with 0.5 PFU of vA5L-Cyan and 0.5 PFU of vA5L-Yellow. After 12 h, the cells were monitored using confocal
microscopy. In row D, the field contains one infected cell with factories and parts of several uninfected cells.
Meet the Mimivirus, the largest known virus
Mimivirus
~1,200 kbp
~1000 genes
Mimivirus genome is twice as large as that of
Mycoplasma genitalium (580 kbp; ~500 genes)
Take home message is that although NCLDV are
huge, they are rank-and-file dwellers
of the Virus World proper
Marine metagenomics has discovered a multitude
of novel NCLDVs related to Phycodnaviruses,
Mimiviruses, and even African swine fever virus
Virus
World
DNA Empire (DdDp; RCE; DdRp)
dsDNA
Herpesvirales
Baculoviridae
Polydnaviridae
Nimaviridae
Nudivirus
RNA-primed
Nucleo-cytoplasmic large DNA viruses (NCLDV)
Corticoviridae
Lipothrixviridae
Caudovirales
Virophages
Narnaviridae
Ourmiaviridae
+RNA
Nidovirales
Flavivirus-like
superfamily
Cystoviridae
Partitiviridae
Picobirnaviridae
-RNA
Mononegavirales
Ophioviridae
Reoviridae
Hypoviridae
Arenaviridae
Tenuivirus
Varicosavirus
Orthomyxoviridae
Bunyaviridae
Protein-primed
Tectiviridae
Adenoviridae
Picovirinae
Fuselloviridae
Rudiviridae
Papillomaviridae
Parvoviridae
Anelloviridae
Polyomaviridae
Rolling-circle
replicons
Microviridae
Nanoviridae
Inoviridae
ssDNA
Circoviridae
Geminiviridae
Picornavirus-like
superfamily
Leviviridae
Viroids, Virusoids,
Hepatitis δ
Bicaudaviridae
Ampullaviridae
RNA Empire (RdRp; Rz)
Alphavirus-like
superfamily
Plasmaviridae
Globuloviridae
Retroid Empire (RdDp; DdRp)
Totiviridae
Chrysoviridae
Birnaviridae
dsRNA
Reverse
transcription
+RNA
Retroviridae
dsDNA
Caulimoviridae
Hepadnaviridae
Recommended reading
Boyer et al. (2009) Giant Marseillevirus highlights the role of amoebae
as a melting pot in emergence of chimeric microorganisms.
Proc Natl Acad Sci U S A 106:21848-21853