J. gen. Virol. (I975), 27, t35-149
I35
Printed in Great Britain
A Classification of Virus Groups Based on the Size of the
Particle in Relation to Genome Size
By R. E. F. M A T T H E W S
Department of Cell Biology, University of Auckland, Auckland, New Zealand
(Accepted 6 January I975)
SUMMARY
For 59 different viruses, when the amount of nucleic acid in the particle is
related either to the dry weight of the particle or to the particle volume, two
classes of virus groups emerge - those with enveloped or those with geometrical
particles.
The enveloped viruses have particles with the following properties: (i) about
4o × Io n daltons of anhydrous weight per Io n daltons of nucleic acid; (ii) a
particle volume of about 2 × io 5 nm 3 per I o ° daltons of nucleic acid; (iii) a limiting
lipoprotein membrane. These properties are qualitatively and quantitatively close
to those of prokaryotic cells.
The geometric viruses have particles with roughly one-tenth the anhydrous
mass per unit of nucleic acid and one twenty-fifth the particle volume per unit of
nucleic acid. They do not possess a limiting lipoprotein membrane.
INTRODUCTION
In the various classifications of viruses that have been proposed the choice of characters
in the hierarchy has been quite arbitrary, and, among the characters used to make the major
subdivisions, there has been no natural reinforcement of one property by another. Where
virus size has been considered as a parameter, only linear dimensions have been used.
Thus Lwoff and his colleagues used the possession of D N A or RNA for the first division
in their classification; capsid symmetry for the second; and the presence or absence of an
envelope for the third (Lwoff, H o r n e & Tournier, I962; Lwoff & Tournier, I97I ). Melnick
0973) used the same divisions for his most recent classification of animal viruses. The
diameter of the virus particle and the mol. wt. of the nucleic acid were the 7th and 8th parameters used by this author. Davis et al. 0973) in their table listing characteristics of viruses
use the symmetry of the capsid for the first division; then the presence or absence of an
envelope; then the presence of D N A or RNA.
In the first report of the International Committee on Classification and Nomenclature of
Viruses (Wildy, I97I) the 43 virus groups described are arranged according to the nucleic
acid content of their particles. The cryptogram (a summary of 'important' virus features)
contains no information on membranes or lipid content. Indeed the cryptogram subcommittee dismissed a suggestion that the presence or absence of lipid should be included
(Wildy, I970.
In this paper I wish to show that when the mol. wt. of nucleic acid in the particle is related
either to the dry weight of the particle or to the particle volume (nm a) two classes of virus
groups emerge. One of these classes possesses a lipoprotein envelope. The other does not.
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136
R.E.r.
MATTHEWS
Table I. Data for the groups of enveloped viruses and some prokaryotes
Virus group
or cell
Nucleic
acid
mol. wt.
(× lO-6)
Particle
mass
(dry)
( x io -e)
Particle
dimensions
(nm)
Particle
volume
(nm 3)
lipid
by wt.
Escherichia eoli
5000
Dialisterpneumosintes 750
1"5 × IO5
1.6 × lO4
lO9
500 × 500 × IO00 I'95 × I08
7
22
Mycoplasma
5o0
2"4 x 1o4
5oo
6'5 × lo 7
IO-ZO
Psittacosis group
Poxvirus (vaccinia)
Herpes virus (herpes
simplex)
400
16o
82
I.I × lO4
3200
2700
450
270 × 270 × I40
18o
4"7 x io 7
I0 × 106
3"0 x lO6
47
5"6
22
27
-
-
Paramyxovirus (NDV)
6
660
x50
1"7 × IO~
Leukovirus
Rous (dry)
Rous (hydrated)
4"2
4"2
294
294
90
I5O
3"8 × Io 5
I '76 X IOn
Rhabdovirus (VSV)
3"5
I7O
17o x 75 diam.
7"4 x I o6
2o
Alpha virus
(Sindbis)
3"0
53
7°
1.8 × lO5
26
Flavi virus
(Dengue type I)
Myxovirus
(influenza)
3"0
43
50
6"5x lO4
Present
3"0
250
Ioo
5"2 x to e
18"5
- 3I~
t
References
McQuillen (I965)
Loewy & Siekevitz
(1969)
Loewy & Siekevitz
(I969); Davis et al.
0973)
Moulder (I964)
McAuslan (I969)
Davis et aL (1973);
Wagner et al.
(1974); Russell,
Watson & Wildy
(1963)
Wildy (1971);
Scholtissek,
Drzeniek & Rott
(1969)
Harvey (1973);
Bellamy, Gillies &
Harvey (1974);
Quigley, Rifkin &
Reich (I971)
Howatson (197o);
Wildy (1971);
Knudson (1973)
Wildy (i97i);
Harrison et al.
(I971);
Pfefferkorn &
Hunter (1963)
Wildy (197I)
Green (1969)
METHODS
Volume calculations. The volumes of all the particles required for infectivity were added
together when calculating the volume of multiparticle viruses and the total amount of
nucleic acid required for infectivity was used to calculate mol. wt. of nucleic acid. For viruses
with tails, total volume was estimated.
Groups of viruses considered. Wildy 0971) lists 43 virus groups. There are sufficient data
for calculations to be made for 4o of these. The data for these groups and 19 additional
groups are given in Tables I to 4. The definition of virus groups is sometimes quite arbitrary
in the present state of knowledge. Most of the viruses considered are the best-studied examples of big groups of viruses whose members share all the properties being discussed
(e.g. one rhabdovirus, VSV). However, reovirus and two other double-stranded R N A viruses
are included. Two rather different iridescent viruses have also been listed.
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A classification using virus and genome size
137
RESULTS
Two classes of viruses
When the dry mass of the virus particles (in daltons) is plotted against mol. wt. of their
nucleic acid (in daltons) two classes e m e r g e - those bounded by a lipoprotein membrane
and those without such a membrane (Fig. I). The same two classes are apparent when the
volume of the virus particles (nm 3) is plotted against the mol. wt. of their nucleic acid (Fig. 2).
The lines in Fig, r and 2 were drawn by inspection. They have a slope of I-0 and are intended
to assist in identifying the two classes of viruses.
I shall use the term enveloped for those viruses which possess an external lipoprotein bilayer membrane which is necessary for the integrity of the particle. As noted below, certain
particles containing lipid are excluded from this class.
Enveloped virus particles have a particle dry mass of roughly 40 × I06[I06 daltons of
nucleic acid, and a particle volume of approx. 2 × lO5 nmZ/Io 6 daltons of nucleic acid. The
four prokaryotic cells shown in Fig. I and 2 have similar values for these parameters.
In contrast, particles of viruses without a limiting lipoprotein envelope (geometrical
viruses) have roughly one-tenth the particle dry mass, and one twenty-fifth the volume, per
unit of genetic material possessed by the enveloped viruses and the prokaryotic cells.
There is probably substantial error in the estimates of volume for some of the enveloped
viruses since estimates have been made on dried preparations. The extent of this error is
indicated by recent data for hydrated RSV (Table I, Fig. 2). It is possible that when diam.
in solution have been estimated for the alpha, flavi and herpes viruses, that similar corrections may be made that will bring these viruses more closely into line with others of the
enveloped class.
The volumes for the geometrical viruses are also based on measurements made in the dry
state. These may also be substantially in error, at least for the larger viruses that possess an
outer layer of protein subunits surrounding an inner core. The possible magnitude of such
error may be judged from the data for reovirus, where we have an accurate determination
of the diam. in aqueous solution (Harvey, ~973) (Fig. 2).
Inspection of Fig. I and 2 shows that the enveloped virus particles fall into two subclasses: (a) those with double-stranded D N A and (b) those with single-stranded RNA.
Fig. I and z also show that the geometrical viruses fall naturally into three subclasses: (i)
all the virus particles that contain double-stranded nucleic acid (DNA or RNA) have
a nucleic acid content/> 3"4 × lO6 daltons; (ii) all the virus particles that contain singlestranded nucleic acid (DNA or RNA) have a nucleic acid content ~< 4"1 × lO6 daltons; (iii)
the viruses with rod-shaped particles that cluster near the single-stranded icosahedral
viruses. These viruses tend to have a high volume or particle mass per unit of nucleic acid
because of the less efficient packing of nucleic acid by protein subunits in a helical array,
compared with icosahedrat. This can be illustrated by comparing TMV and TYMV. Both
have single-stranded R N A with a mol. wt. of about z.o x lO6. The coat protein subunit of
TMV has a mol. wt. of 17 5oo, while that of TYMV has a tool. wt. of 2o ooo. TMV has a dry
particle mass of 39.o × Io 6. For TYMV the dry mass is 5"4 × Io6. TYMV RNA, reconstituted in vitro with TMV protein produces a rod with the dimensions of TMV (Matthews,
1966).
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x38
R.E.F.
MATTHEWS
T a b l e 2. D a t a f o r the groups o f geometrical viruses containing
double-stranded nucleic acid
Mol.
Wt.
of
Particle
nucleic dry
acids
mass
Virus g r o u p
( × 10 -6) ( × 10 -6)
Iridovirus R M I V
(mosquito)
T2
464
2750
I3O
325
~5CbK
130
230
F r o g virus 3
I3O
430
Iridovirus (Tipula)
IO5
55I
8o
Lambda
Particle
dimensions
(nm)
215"
Particle
volume
( n m 3)
5'15 × 106
Head
34"6 x lO4
95 × 65 diam.,
tail
I 0 0 × 20 diam.
Head
_~ 6.2 x io ~
195 × 62, tail
275 long
135
1 "28 × lO6
13o
I ' I 4 x lO 6
-~ 65o
4oo × 7o
1.5 x lO 6
33
66
L-PPI
T7
27
25
68
130
H e a d 64, tail
165 x 13"6
59
H e a d 47,
tail
P2
22
--
Adenovirus
22
183
PM2
Reovirus (dry)
I8
15
129
130
Reovirus (hydrated)
Wound turnout
virus
Insect cytoplasmic
polyhedrosis
Bacteriophage ~29
15
15
I3O
7I
98
70
4"9 X 106
1.8 x to ~
15
54
65
II
18
Baculo (nuclear
polyhedrosis
Lipid
(~o by
weight)
References
3"9 W a g n e r et al. (I973)
o
M a t t h e w s (I969)
o
A g a b i a n - K e s h i s h i a n & Shapiro
(197o)
14
L u n g e r & C a m e 0 9 6 6 ) ; Smith &
M c A u s l a n (I969); T a n &
M c A u s l a n (197I)
9
K a l m a k o f f & T r e m a i n e (I968);
Kelly & A v e r y (1974); Kelly &
Vance (I973)
o-2 Bergold & Wellington (1954);
Wildy (I971); 13ellett et al. (1973)
Bombyx)
16-I × lO5
o
Bayer & B o k a r o v ( 1 9 7 3 ) ; M a t t h e w s
(1969)
B r o w n (1972)
A d a m s (1959; D a v i s o n & Frieii~lder (1962); Studier (1972).
1"O7 x IO5
5"5 x ~o4
O
o
I. 3 x io ~
o
Barrett et al. (I973)
I7-8 × IO4
o
6o
I'13 x io 5
io
Pifia & G r e e n (1965); G r e e n et al.
i967); Wildy (i971)
Espejo & Canelo (I968)
75
2'2 × IO 5
I n × 15
H e a d 58,
tail
135x I7
7o
0t
o(
H a r v e y (I973); W o o d (I973);
Farrell, H a r v e y &]3ellamy (1974)
o
W o o d (1973)
1-43 × ro~
o
W o o d (1973)
2"5 x 1 0
o
A n d e r s o n , H i c k m a n n & Reilly
(1966); R u b i o et al. (1974)
7"5 x lO4
o
Barrett et al. (I973)
7'7 × lO4
o
Wildy (I97I); G r e e n (1969)
Shepherd (I97O); Shepherd,
B r u e n i n g & W a k e m a n (197o);
Bellett et aL (1973)
Wildy (I971)
P4
6"7
--
Papillomavirus
(Shope rabbit)
Caulimovirus
5
4o
Head
32 × 3I,
tail 32 × 6
H e a d 44,
tail 135 × 17
53
4"5
28
50
6"5 × IO4
o
3"4
26
43
4 ' 1 2 × 104
0
Polyoma
* M e a n value between t h o s e for stained a n d thin section preparations.
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A classification using virus and genome size
I39
Table 3- Data for the groups of geometrical viruses containing
single-stranded nucleic acid
Virus group
Nucleic
acid
Particle
mol. wt. drymass
( x i o -6) ( x 1o -6)
CpMV
NEPO
BBWV
CMV
4-t
3"7
3"5
3"4
t3'7
lO'6
11'5
5"5
AMV
3.0
18.2
CaI~ci
PEMV
~ 3.0
2"9
7'0
I 1'7
TSV (assuming
3 largest RNAs are
needed)
BMV
Entero
Cardio
Equine rhino
Foot and mouth
H u m a n rhino
Acute bee paralysis
2.8
t8.1
2.8
2.6
2.6
2.6
2-6
2'2
2.o
I4'o
8"5
8"5
8"3
8"4
8"4
6-7
Parvovirus
2"o
TYMV
¢X174
Particle
dimensions
(nm)
Particle
volume
(nm ~)
Lipid
( % by
weight)
References
28 ( x 2)
27.5 ( x 2)
2'3 x 1o4
2.3 X 10*
o
0
27(×2)
28 (X 3)
2 ' I 2 X IO4
3-5X 104
0
58X 18;
3.19X i 0 4
0
Brown & Hull (1973)
Brown & Hull (1973)
Brown & Hull (1973)
Brown & Hull (1973);
Lot et al. (I974)
Bos & Jaspars (1971)
2'24 X 1 0 4
2"3I × I04
o
o
Brown & Hull (1973)
Hull & Lane (1973)
2"8 x lO4
o
Fulton (1971); Ghabrial &
Lister (1974)
2'76 x I04
Brown & Hull (1973)
Brown & Hull (1973)
Brown & Hull (1973)
Brown & Hull (1973)
Brown & Hull (1973)
Brown & Hull (1973)
Brown & Hull (1973);
Bellett et al. (1973)
Tinsley & Longworth (I973);
J. F. Longworth (personal
communication)
Brown & Hull (1973)
Matthews (1969); Spencer
et al. (I972); Wildy (197I)
Tinsley & Longworth (I 973);
Wildy (I97 I)
Brown & Hull (1973)
Brown & Hull (1973)
Brown & Hull (1973)
Brown &I-lull (1973)
Brown & Hull (1973)
Kassanis (I97o)
49× I8;
38 x 18
3S
29 and
27
approx.
3 particles
largest
28
26 ( x 3)
0
28
28
28
24
28
29
1"15 X 104
I'15 X 10 4
I ' 1 5 X 104
o,72 X 104
I'15 ~ 104
I'27 % 104
o
o
o
o
o
o
o
5'4
22
o.55 X lO4
o
2.0
1"7
5"4
6.8
28
25
I"15× lo 4
o,81 >~1o4
o
o
Latent rat
1.62
4"7
2I
0'48 X IO4
o
TBSV
TNV
SBMV
R17
1"6
1%
1-4
9"3
7"0
6'3
30
26
28"5
1'4× 104
o,92 x IO4
1,2 x I0 i
I-1
1.1
3"6
4"2
25
25
0'81 g I04
0.81 ~< 104
o
o
0
o
o
0-4
2.0
17
2,6x lO8
o
(Galleria)
Qfl
Satellite
T a b l e 4. Data f o r the groups o f rod-shaped viruses
Virus group
Barley stripe
mosaic virus
Carla viruses
TRV
Potato X virus
TMV
fd virus
Nucleic Particle
acid
mass
mass
(dry)
(× 1o6) ( × IO-6)
Particle
dimensions
(nm)
Particle
volume
(nm")
References
3'8
95
3 8 7 x 2 o ( × 3)
I2X IO4
Lane (1974)
3"6
3"6
2"1
60
79
35
65ox 12
305 x 25
515 x 13
7 x lO4
15 x lO4
7 x 104
2-o
39
3oox I8
7 - 6 x IO 4
1"9
I6
88OX5
1'7 x I04
Wetter (197 I)
Harrison (197o)
Bercks (197o)
Klug & Caspar (196o)
Frank & Day (x976); Ray
(1968); Matthews (1969)
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I40
R. E. F. MATTHEWS
I
I
!
I
E. coli
/
1011
Mycoplasma ( 7 ~
10~°
PsittaDialister
109
Paramyxo
/
®/
/
O
Rous
/
/
_
Rhabd~/
_
.X_X/
/;
108
Alpha
, X xx
Flavil~Ik~x
X/
• ..{
I0?
106
105
x
. .,,"
I
106
I
I
I
107
10s
109
101°
Mol. wt. of nucleic acid
Fig. I. Relationship between mol. wt. of nucleic acid and dry mol. wt. of particle for 59 groups of
viruses and four prokaryotic cells. Q, cells and enveloped virus particles. The names of these are
indicated, x, unenveloped virus particles containing double-stranded nucleic acid. I , viruses
with unenveloped rod-shaped particles. 0, viruses with unenveloped icosahedral particles containing single-stranded nucleic acid.
Some other properties of the enveloped and geometrical classes of viruses
Presence of lipid
All the enveloped virus particles contain lipid, usually 20 to 30 % by weight (Table I).
None of the geometrical virus particles containing single-stranded nucleic acid have been
reported to contain lipid. Five of the geometrical viruses have been shown to contain some
lipid (Table 2). However, in these, the lipid does not form an outer bilayer membrane. It is
present as a smaller proportion of the dry weight of the particle than found for the
enveloped viruses (except poxvirus). Where it has been studied the composition of the lipid
in the geometrical viruses differs significantly from the host lipid and much of the lipid is
synthesized during virus maturation (e.g. Tsukagoshi & Franklin, I974).
Frog virus 3 (FV3) and similar viruses have very large icosahedral particles which appear
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A classification using virus and genome size
109
I
I
I4I
I E. coli
I
Mycoplasma
108
Dialist
Psittacosis
107
S
106
Myxo . . ~
Rhabdo
"ha~~Rous
/Alpha(~
/×
I
/
(D)
x
" ~x ×
lOs
Flavi I ( ~ xx
.e
104
/
°
I
lOs
lO6
e
X
,I
I,,
107
!
108
I
109
10t°
Mol. wt. of nucleic acid
Fig. 2. Relationship between tool. wt. of nucleic acid and volume of particle (nm3) for 59 groups of
viruses and four prokaryotic cells. G, ceils and enveloped virus particles. The two circles joined
by a vertical line are for Rous hydrated (upper) and Rous dry (lower). x, unenveloped virus
particles containing double-stranded nucleic acid. The two x joined by a vertical line are for
reovirus hydrated (upper) and reovirus dry (lower). I , viruses with unenveloped rod-shaped
particles. O, viruses with unenveloped icosahedral particles containing single-stranded nucleic acid.
to acquire an envelope derived by budding from the plasma membrane (Darlington, Granoff
& Breeze, I966). Nevertheless particles purified from disrupted infected cells are not enveloped but are infectious (Hauts, Gravell & Granoff, I974). Thus, the membrane is not an
essential part of the virus particle. On other properties they fit well in the non-membrane
bound class. The 14 ~ lipid found in unenveloped FV3 particles is probably an integral part
of the virus as it is in PM2 (Harrison, Caspar, Camerini-Otero & Franklin, ~971 ; Willis &
Granoff, I974).
The baculoviruses are frequently referred to as having a membrane, but this appears to
consist of a stacked disc array of protein subunits (Bellett, Fenner & Gibbs, I973) and
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I42
R. E. F. MATTHEWS
Table 5. S o m e e n z y m e s f o u n d in viruses
Virus or group
Pox viruses
Herpes virus
Paramyoxvirus
Leukovirus
Rhabdovirus
Myxovirus
Iridoviruses
T2 virus
Reoviruses
Frog virus 3
Adenovirus
Polyoma group (SV4o)
A. Enveloped groups
Enzymes
DNA-dependent RNA polymerase
Nucleotide phosphohydrolase
Protein kinase
Endonuclease; Exonuclease
Terminal riboadenylate transferase
Protein kinase
RNA-dependent RNA polymerase
Protein kinase
RNA-dependent DNA polymerase
DNA ligase
Exonuclease
RNA-dependent RNA polymerase
Protein kinase
RNA-dependent RNA polymerase
B. Geometrical groups
RNA polymerase
ATPase; lysozyme
RNA-dependent RNA polymerase
Nucleoside triphosphatases
Two endodeoxyribonucleases
Endoribonuclease
Nucleotide phosphohydrolase
Adenosine triphosphate
phosphohydrolase
Endonuclease (DNA)
Endonuclease
References*
Kates & McAuslan (1967)
Gold & Dales (I968)
Kleinman & Moss (I973)
Aubertin & McAuslan (I972)
Brown, Dorson & Bollum (1973)
Randall et al. 0972)
Huang, Baltimore & Bratt (I97I)
Roux & Kolakowski 0974)
Mitzutani & Temin 0970
Mitzutani et al. (I970
Chang et at, (I974)
Imblum & Wagner (2974)
Bishop et al. (I972)
Kelly & Tinsley (1973)
Matthews (I969)
Zweerink, Ito & Matsuhisa (I972)
Kapuler et aL (197o)
Kang & McAuslan (1972)
Vilagines & McAuslan Ct971)
Aubertin et al. (t97I)
Burlingham et al. (1971)
Kaplan, Wilbert & Black (I972)
* References are not necessarily to the first report for a particular enzyme,
contains only I. 3 ~ lipid (Bergold & Wellington, I954), although a more recent estimate
gives 3"7 ~ (Bergold, I963).
The presence o f e n z y m e s in the virus particle
Members of the enveloped virus groups (except alpha and flavi) have been shown to contain enzymes concerned with nucleic acid metabolism (Table 5).
Large viruses in five of the geometrical groups containing double-stranded nucleic acid
(and one small virus of the polyoma group) have been shown to contain enzymes as part
of their structure (Table 5)With one exception, none of the geometrical viruses containing single-stranded nucleic
acid have been shown to contain enzymes. The exception is a parvovirus, Kilham rat virus
(Salzman, I97I). However, there was no convincing demonstration that the D N A polymerase activity reported in the virus preparations was an integral part of the virus particle
rather than a host contaminant.
W a t e r content
I f enveloped viruses bound, on average, 2"5 times as much water as geometrical did this
would account for the average difference in Fig. I and 2 between the two classes (tenfold on
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A classification using virus a n d g e n o m e s i z e
I43
Table 6. Water content or solvation o f some cells and viruses
Cell or virus
Water
content
(ml/gm dry
matter)
Hydrodynamic
radius
(nm)
References
Cells
Escherichia coli (with wall) 3'0
E. coli (without wall)
4"0
Dialister pneumosintes
3"o
RSV
AMV
2'7±0. 9
4"3!I'2
Davis et al. (I973)
Davis et al. (I973)
Loewy & Siekevitz 0969)
Enveloped viruses
74'o
J.D. Harvey (personal communication)
8o-o
J.D. Harvey (personal communication)
REO
T7
PM2
Caulimovirus
Geometrical viruses with double-stranded nucleic acid
1"5
49"0
J.D. Harvey (personal communication)
1-18+ o.o6
33"3
Camerini-Otero et al. (I974)
1. I ___0.08
33"0
Camerini-Otero et al. (I974)
1.7
28'4
J.D. Harvey (personal communication)
RI7
Off
BSV
TYMV
TSV B component
M component
T component
Geometrical viruses with single-stranded nucleic acid
Camerini-Otero et al. (1974)
I'O2_O'O9
I4-o
Camerini-Otero et al. (I974)
I'22+O'O8
15"I
Camerini-Otero et al. (1974)
O'75+_O'O4
I7'2
J. D. Harvey (personal communication)
o'78
14'7
J. D. Harvey (personal communication)
1'o9
17-4
J. D. Harvey (personal communication)
I'I2
I6-2
J. D. Harvey (personal communication)
I'26
15"4
a dry mass basis and 25-fold on a particle volume basis). The 20 to 30 % (on dry weight) of
lipid would make a contribution of only a few per cent to the hydrated volume of the
enveloped viruses. The water content of viruses has not received a great deal of attention.
However, with the development of new methods for the rapid and accurate measurement of
hydrodynamic radii new informaton is becoming available (Table 6).
The error in these values is large even for the recent measurements and many more viruses
require study. Nevertheless, the enveloped particles that have been studied have a water
content like that of prokaryotic cells. Most of the geometrical virus particles for which
data are available have about half as much water per unit dry matter.
Multiple genomes within a single envelope
A proportion of particles containing more than one genome within a single membrane
has been found for the following groups of enveloped viruses: pox, herpes, paramyxo,
myxo, leuko and alpha viruses (Simon, I972). The phenomenon appears not yet to have
been established for the rhabdo- and flaviviruses. In general the phenomenonen does not
occur in the geometrical viruses, although the long rods of the F f bacteriophage provide
an analogous phenomenon (Simon, I972 ) and some baculoviruses may contain up to
about 2o nucleocapsids within one outer protein membrane.
Exceptions
On the size data at present available, the alpha and flavi groups occupy an intermediate
position as indicated in Fig. I and 2. They are also anomalous in that the virus particles do
not appear to contain enzymes concerned with nucleic acid metabolism.
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R . E . F . MATTHEWS
144
A. Enveloped viruses
Single-stranded
Double-stranded
RNA
DNA
/\
f
Pox
Herpes
No DNA step in
viruses
viruses
replication cycle
genomecomplementary
~
Alphaviruses
DNA step in
replication cycle
-....
genome = m R N A
/
--...
J
to mRNA
Flavi-
Rhabdo- Paramyxoviruses
viruses
viruses
Myxo- RNA tumour
viruses
viruses
B. Geometrical viruses
Double-stranded
nucleic acid
Single-stranded
nucleic acid
/\
particles)
/
\
DNA RNA
lcosahedral
particles
/\
DNA RNA
Helical
rods
/\
DNA RNA
Fig. 3. Summary of suggested divisions for groups of viruses.
Some cultures of tobacco ringspot virus (TRSV) contain a satellite virus (S-TRSV) which
uses the TRSV coat protein built into a shell identical to that of TRSV. S-TRSV belongs
to the geometrical class since it does not have a lipoprotein envelope. However, it is anomalous with respect to its nucleic acid. The R N A of S-TRSV has a mol. wt. of 1"2 × Io 5 and
I2 to 25 pieces of this size are encapsulated within a TRSV protein shell (Schneider, Hull &
Markham, 1972; Sogo, Schneider & Koller, I974). N o other example of this situation is
known. S-TRSV may represent a satellite 'viroid' which uses the protein shell of the virus
upon which it is dependent. The high resistance to u.v. inactivation (Diener, Schneider &
Smith, I974) supports the view that the amount of R N A required for infectivity is very
small.
DISCUSSION
On the basis of the data outlined above, I suggest that the primary division of the viruses
should be into two classes:
A. Enveloped virus particles with the following properties, which resemble those of
prokaryotic cells:
(I) Bounded by a lipoprotein membrane.
(2) A particle volume per unit of genetic material of the order of 2 × IO5 nma[I@ daltons
of nucleic acid, and a dry particle mass of 4 ° x lO8 daltons, per lO6 daltons of nucleic acid.
(3) A water content in the range 3 to 4 ml/g dry matter.
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A classification using virus and genome size
I45
(4) Presence of enzymes concerned with nucleic acid metabolism, except in togaviruses.
(5) Occasional occurrence of more than one genome within a single envelope.
B. Geometrical virus particles with the following properties:
(I) No limiting lipoprotein membrane.
(2) A particle volume per unit weight of nucleic acid about one twenty-fifth, and a dry
particle mass per unit weight of nucleic acid about one-tenth, that of the enveloped class.
(3) Following from (2) they will have an expected water content of about 1.5 ml/g dry
matter.
(4) The absence of enzymes from the virus particle except for the larger members of the
class.
(5) No multiple genomes within a single envelope (except for some baculoviruses).
Further subdivisions of the two classes
A grouping of animal viruses according to the strategy of their genome has been proposed
(Baltimore, i97i ; Subak-Sharpe, I97I) and has been recently reviewed for the RNA viruses
by Shatkin (i974). The enveloped viruses containing single-stranded RNA are readily
subdivided according to the strategy of their genome (Fig. 3A).
As noted earlier, the geometrical viruses appear to fall naturally into three subclasses.
These suggestions are summarized in Fig. 3 B.
The differences between the enveloped and geometrical classes can be highlighted by considering influenza virus. Although it is about three orders of magnitude smaller than Eseherichia coli it has a similar dry mass and particle volume per unit of nucleic acid. On the other
hand influenza virus contains about the same amount of RNA as enteroviruses and yet
has roughly Io times the dry mass and 20 to 30 times the particle volume. A proportion of
the increased dry mass will be due to the presence of the lipoprotein envelope, but substantial amounts of other proteins must be present as well.
There appears to be no biological or structural reason why such additional proteins should
be a necessary consequence of the presence of a bilayer membrane. The greater dry mass
per unit of nucleic acid may therefore be regarded as an independent property. However,
a larger proportion of water in enveloped viruses might well result directly from the
presence of a membrane with osmotic properties.
Several lines of investigation could further test the validity of the classification. These
include: (i) Careful re-examination of the size in solution (using laser light beat spectroscopy) of
various virus groups, such as herpes-, alpha- and flaviviruses. Substantially larger particles than
the published estimates could be expected. (ii) Accurate determination of the water content
of many virus particles for which information is lacking at present. (iii) Re-investigation of
the DNA polymerase activity reported for Kilham rat virus. (iv) Further structural studies
on the icosahedral cytoplasmic deoxyriboviruses and the baculoviruses to delineate more
clearly to which class they belong.
A primary division of viruses into the two classes outlined above would have greater
predictive value than current schemes and might perhaps correspond more closely to
evolutionary origins.
Wildy (1973) drew attention to the long tradition of separatism of the four main' branches'
of virology, and he gave a summary of current information on possible bridging groups of
viruses. A classification based on the divisions indicated in Fig. 3 would give substantial
unity to virology as a whole, as it relegates categories based on host organisms to a subsidiary position.
io
VIR
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27
146
R.E.F.
MATTHEWS
I w i s h t o t h a n k A . R . B e l l a m y , J. D . H a r v e y , J. K a l m a k o f f ,
Miles for most useful comments and discussion.
J. L o n g w o r t h
a n d J. A . R
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