INTERNATIONAL JOURNAL OF
SYSTEMATIC
BACTERIOLOGY
Vol. 16, No. 2
A p r i l 1966
pp. 223-252
REVISION OF THE FAMILY CHLAMYDIACEAE RAKE
(RICICETTSIALES): UNIFICATION O F THE PSITTACOSISLYMPHOGRANULOMA VENEREUM-TRACHOMA GROUP
O F ORGANISMS I N THE GENUS CHLAMYDIA JONES,
RAKE AND STEARNS, 1945'
L.A. P a g e
U. S. Department of Agriculture, A g r i c u l t u r a l R e s e a r c h
S e r v i c e , Animal D i s e a s e and P a r a s i t e R e s e a r c h Division,
National Animal D i s e a s e L a b o r a t o r y , A m e s , Iowa
ABSTRACT. S i n c e 1 9 4 5 , t a x o n o m i s t s h a v e m a d e
no l e s s than seven attempts t o define the bact e r i a of t h e f a m i l y C h l a m y d i a c e a e R a k e w h i c h
i n c l u d e s t h e e t i o l o g i c a g e n t s of p s i t t a c o s i s ,
lymphogranuloma
venereum, and trachoma.
T h e s e b a c t e r i a a r e o f t e n d e s i g n a t e d by t h e
v e r n a c u l a r t e r m , P L T g r o u p of a g e n t s . C l a s s i f i c a t i o n s w e r e p r o p o s e d b y M o s h o v s k y (1945),
R a k e (1 9 4 8 , 1 9 5 7 ) , K r a s i l ' n i k o v (1 9 4 9 ) , Z h d a n ov and Korenblit
(1949), Rhyzkov (l950),
Zhdanov (1953) and Levaditi, Roger and Destombes (1964).
The result was to increase
t h e n u m b e r of g e n e r a f o r t h e P L T g r o u p c u l m i n a t i n g i n t h e L e v a d i t i Et a l . p r o p o s a l o f
four genera for this bacterial group: Chlamydia Rake, Miyagawanella Brumpt, Bedsonia
Meyer, and Rakeia Levaditi, Roger and Destombes.
Evidence for continued recognition
o f t h e s e g e n e r a w a s e x a m i n e d i n t h e l i g h t of
r e c e n t k n o w l e d g e of P L T o r g a n i s m s , a n d t h e
v a l i d i t y of e a c h n a m e a c c o r d i n g t o t h e r u l e s
o f t h e I n t e r n a t i o n a l C o d e of N o m e n c l a t u r e o f
On
Bacteria and Viruses was ascertained.
the grounds that the taxonomic significance
o f p r o p e r t i e s c o m m o n t o b a c t e r i a of t h e P L T
In addition t o t h e authpr, t h e following m e m b e r s of t h e
Subcommittee on the Chlamydiaceae of the A m e r i c a n Society
f o r Microbiology's Taxonomy Committee have reviewed the
m a n u s c r i p t and support the proposal: F. B. Gordon, J. W.
Moulder, E. J a w e t z , and M. P o l l a r d .
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
224
I N 'T
Ra A.
T I0 N A L
J OU R N A L
group (morphology, developmental cycle and
g r o u p a n t i g e n ) o u t w e i g h e d t h e v a l u e of t h e
characteristics that separated the various
species or strains (host preferences and spec i f i c a n t i g e n i c i t y of l i p o p r o t e i n s of t h e c e l l
w a l l ) , i t w a s c o n c l u d e d t h a t a l l of t h e s p e c i e s
of b a c t e r i a o f t h e P L T g r o u p p r o p e r l y b e Therefore, their
longed in a single genus.
unification in the genus Chlamydia Jones,
Rake and Stearns , 1945, is proposed.
The
validly published g e n e r i c name Chlamydia replaces Miyagawanella Brumpt 1938 which wa s
not validly published and has p r i o r i t y o v e r
Bedsonia Meyer (1953) and Rakeia Levaditi,
Roger and Destombes (1964).
Furthermore,
the t e r m "virus" i s incorrect and misleading
when applied to thes e bacteria.
The development of a generally acceptable nomenclature
f o r o r g a n i s m s of the psittacosislymphogranuloma venereumt r a c h o m a ( P L T ) group h a s been hindered by s e r i o u s d i s a g r e e m e n t among microbiologists a s t o the c o r r e c t name
f o r these bacteria. In the l a s t two decades, no l e s s than
seven a t t e m p t s , including t h r e e repetitive ones , have been
made t o define and name the m e m b e r s of the PLT group
within the f a m i l i e s Chlamydozoaceae and E h r l i c h i a c e a e
(Moshkovsky, 1945) o r Chlamydiaceae (Rake, 1957) while
the number of g e n e r a proposed by various authors h a s inc r e a s e d f r o m Moshkovsky's original two to ten, s o m e of
which r e p r e s e n t proposals of synonyms (Table 1).
F o r the m o s t p a r t , the new g e n e r i c names appeared,
along with additional species n a m e s , i n each new emendation
of descriptions (Chlamydozoon, E h r l i c h i a Moshkovsky, 1945;
Rickettsiaformis Zhdanov, 1953; Chlamydia Rake, 1957;
Rakeia Levaditi, Roger and Destombes , 1964; Colesiota
Rake, 1948, Ricolesia Rake, 1957, and Colettsia Rake, 1957,
the l a t t e r t h r e e g e n e r a being f o r Coles' conjunctivitis organisms.
T h r e e distinct proposals f o r g e n e r i c n a m e s w e r e
made a p a r t f r o m any attempt to c i r c u m s c r i b e the group as
a whole a s inMiyagawanella Brumpt, 1938, Chlamydia J o n e s ,
Rake and S t e a r n s , 1945, and Bedsonia Meyer, 1953).
T h i s proliferation of names m o s t of which a r e synonyms
h a s produced understandable r e s t r a i n t , i f not confusion,
among microbiologists i n r e f e r r i n g t o o r g a n i s m s of the P L T
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
SYSTEMATIC BACTERIOLOGY
Table 1 .
225
Condensed classification schema of various
authors for the family Chlamydiaceae (Rake).
(Names are listed as the author listed them
without regard to error)
- .-
-
3) conjunctivae Cobs nom. nov. 3
4) conjunctivet-b&a
C. n~m.
2)
conjunctivae Coles Hosh.
conjunctivae-gai Coke nom. nova
brlichiaceae
..1) EbrUchia
bsh.
lymphogranulomatosis
. Miyag-ellaBrruapt
IymphograuulOnatis.
Brumpt '1)
2) psittaci Lillie
3) broachopneurmniae Mosh.
Br.
2) paittacii L i l l i e
3) ornithosis sp. UOV.
bronchopneumoniae %ah.
other species)
4) c d s (Don. & Lesto.)
5) ovina h a t . & Don.)
6 ) b o d s )Don. & Lesto.)
7) kurlovi (Mosh.)
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
226
INTERNATIONAL JOURNAL
Table 1 (continued)
--.-
Cnlamydla Rake
1 tracEo~EF&p-><&enitale
Mosh.
_lo,I
32-
12.
13.
14.
15*
16.
17.
I
3) conjunctivae Coles Moah.
b) conjunctivae-galli Colts
a) conjunctivae-bovis b s h .
13) conjunctivae
16) kerato-conjunctivae'
3) pecoris manov & bren.
4) pullorum 7&K
18.
19.
20 *
2 L hrlichiaceac
4
:
2 . . Ehrllchia
-.
25. a) lymphogranulometoeis Mosh.
22;
26.
27.
28.
29.
30*
3. d) pnewniae Bergey e t
32.
10) lymJhophilus*
~ l .
*
33.
35.
11 opposum nm. MY.
151 ovia sp. nov.
14) bods ZBdc
%.
37.
38.
39.
40. other species)
41.
42.
43.
44.
45.
46.
47.
48.
492
I
:other species )
5 nrningophilus*
9 mnocytaris*
8 osteophilus*
6 cricetia*
bpparent SP. nov.,
lorn. nov., etc. thou&
lot so designated by
other species)
4) columbarum ~ p nov.
.
6) pneumolncningitidie sp.mv.
9 ) roaentium EP. nov.
Luther.
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
227
SYSTEMATIC BACTERIOLOGY
Table 1. (continued)
iri
Rake (Bergey's 7th) 1956
No.
1.
2.
3.
4.
5.
6.
7.
a.
9.
10.
ll.
12.
13%
i4.
-
15
16.
17*
1s. .
19. .
~
_
MICROTATOBIOI%S Philip
RIMBTTSIALES B u c k & Buch.
a - I E r ~ ~ & b b ; - o o v__-____
r;. ~
2.
~
-
=
a
oculogenitale Mosh.
-
I
'
-
Roger, Destombes 1$4*
~CKE!ITSIALESBuch.-&.J&ch.
lanprdidae L. R- and D.
2. Chlaydioideae (new subfamily)
-
1. C h l m i e a e (new t r i b e )
1. C h l w d i a Rake
1 trachomatfs Busacca
2 oculogenit&e Moeh.
1. Colesiotoideae f n e w subfamily)
--1. Colesioteae (nev tribe)
__
__ ___ ---
2. Colesiota Rake
1 ) c o ~ J u " c t i v a c ~ -!--L--~
---3. Ricolesia gen. nov.
1) conjunctivae Colee comb. nov.
2 bovis Cole8 comb. nov.
31 caprae coles comb. nov.
4 lestoquardii Don. & Gayvt
20.
Leviditi,
-
SCEIZCMYCFPES von Baegeli
mi--
1.
RIILI.
2. R i c o u R a k e
1) conjunctivae &lee Rake
____
2.
--
_
I
_
Colettsieae (new tribe)
-__
-
1) pecoris ~ a k c
21.
22.
23.
24.
25*
26.
27.
28.
29.
30
31.
32.
33.
34.
35.
36*
37.
-
38.
39.
40.
2) fells Rake
9)
opossumi Ryzhkov
10) Oy18 ZManOV
11) b o d s York & Baker
12) pecoris Rake
original names for
subfamilies and t r i k e utilized endings
derived from the Botanical or Zoological
Nomenclature Codes. Tnese endings were
corrected t o proper form according t o
the Bacteriological Code.
43.
44.
45.
46.
47.
48.
49.
1) pecoris Rake
* Ihe authors'
41.
42.
....
--.--
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
228
INTERNATIONAL JOURNAL
group, and many a u t h o rs , even in s y s temat i c studies, have
r e s o r t e d t o the u s e of hyphenated m o n s t r os i t i es abbreviated
as PLV ( p s i t t a c o s i s lymphog ranuloma vene r eum ) or even
P O M P ( Ps i t t a c o s i s ornithosis m a m mal i an pneumonitis)
( T e r z i n , 1958,). The n a m e s applied t o the numerous dise a s e s in b i rd s and mammals caused by t hes e or gani s ms ,
h a s been f u rt h e r complicated:
Me y e r (1940) proposed t he
name "ornithosis'' for the d i s e a s e s of non-psittacine bi r ds
caused by m e m b e r s of the P L T group, hence the etiologic
agents w e r e ornithosis agents. On the presumption that
uniform coding was d e s i ra b l e f o r the grouping of new isol a t e s of o r ga n i s m s causing t ra c h o m a and inclusion conjunctivitis, a group of microbiologists working with t hes e organi s m s have a g r e e d t o a "Nomenclature of i s ol at es of v i r u s
f r o m t r a c h o m a and inclusionblenorrhea" (Gear $ &., 1963).
This terminology involved the u s e of the abbreviation TRIC
f o r TRachoma-inclusion _Conjunctivitis with additional coding f o r immunological grouping, country of origin, isolation
number, t i s s u e of origin, and ultimate diagnosis.
Additional disagreement a l s o e x i s t s on whether to designate P L T o rg a n i s m s a s v i r u s e s , ri c k et t s i ae o r something
n e u t r a l as agents or organisms. A s u m m a r y of the m o s t
recent terminology used t o d e s c ri b e o rgani s ms of t he P L T
group i n t i t l e s of r e s e a r c h p a p e rs published i n the last 5
y e a r s i l l u s t ra t e s the c u r r e n t range of t e r m s (Table 2).
Among the s y s t e m a t i s t s , t h e taxonomic position of the
whole group h a s remained unchallenged; that i s , the P L T
o r g a n i s m s , with m i n o r variation, have been placed i n t he
o r d e r Rickettsiales, s e p a ra t e d by family f r o m the t r u e
r i c k e t t s i a e and c l e a rl y distinct f r o m v i r u s e s as defined by
Lwoff (1957). Recent studies by many w o r k e r s on the m o r phology, cytology, chemical nature and independent metabolism of P L T o rg a n i s m s a s s u m m a ri z ed by Moulder (1964,
1966) h a s produced sufficient evidence t o w a r r a n t recognition of o r g a n i s m s of t h e * P LT group a s bact er i a and not as
viruses.
F u r t h e r m o r e , those committed i n r ecent y e a r s
t o the study of the taxonomy of v i r u s e s have not included
o r g a n i s m s of the P L T group i n that category (Andrewes,
1964; Huck, 1964; Wilner, 1964). Thus, the t e r m v i r u s h a s
become i n c o rre c t and misleading f o r the etiologic agents of
p s i t t a c o s i s , lymphogranuloma venereum, t r achoma and t he
o t h e r d i s e a s e s of m a n or a n i m a l s caused by m e m b e r s of the
P L T group.
In the light of recent well authenticated r e s e a r c h clarifying the relationship of the P L T group t o other or gani s ms ,
-
-
-
-
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
SYSTEMATIC
22 9
BACTERIOLOGY
T a b l e 2. D e s i g n a t i o n i n t i t l e s of j o u r n a l a r t i c l e s f o r P L T
o r g a n i s m s o r c o m p l e x e s t h e r e o f (1960-May
1965)
Indexes* for
1563 1962 1961
Terminology
1965
1964
Psittacosis (virus, group,
agent)*
16
10
8
Ornithosis (virus, group,
agent 1
,
12
Total
15
14
75
4
18
51
5
8
12
12
5
Psittacosis-Ornithosis
(or reverse) virus,
group
1
1
1
Psittacosis-lymphogranuloma
or PLV
3
9
5
1
1
3
3
2
3
Psittacosis-lymphogranulomatrachoma or PLT
2
Ornithosis bedsoniae
2
1
Bedsonia
1
3
2
2
1
1
Trachoma-Inclusion
Conjunctivities
5
8
1
4
1
1
2
2
7
8
13
Neorickettsia o r Pararickettsia
2
2
Bacteria
1
1
8
3
Index Veterinarius, 1961-1964; Index Medicus,
1960, 1963, 1965; Biological Abstracts, 1964-1965.
++
2
1
Miyegawanella
checked in:
3
1
Ornithosis-Lymphogranuloma
* Titles
1960
The term virus was the prevalent uswe.
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
15
2
230
INTERNATIONAL JOURNAL
i t was important that a proposal be developed that was both
taxonomically satisfactory and nomenclaturally c o r r e c t .
The p r e s e n t paper i s such a n attempt.
The t a s k of p r e p a r i n g a proposal which blended the des i r e s of microbiologists f o r convenient terminology with the
r e q u i r e m e n t s f o r c o r r e c t nomenclature consisted of ( 1 ) r e viewing all past proposals of names f o r the taxa of the P L T
group f o r t h e i r validity of publication, legitimacy and c o r r e c t n e s s in accordance with the r u l e s of bacteriological
nomenclature e x p r e s s e d i n the International Code of Nomenc l a t u r e of Bacteria and V i r u s e s ( 1 9 5 8 ) ; ( 2 ) avoiding proposals of new names f o r the taxa of the P L T group on t h e
grounds that a terminology based upon names previously
proposed was preferable.
Selection of g e n e r i c names and
names of type s p e c i e s and s t r a i n s f o r P L T taxa was made
with due consideration of past proposals, c u r r e n t nomenc l a t u r a l needs, and c u r r e n t r e s e a r c h on the P L T group;
( 3 ) the conclusions and recommendations of this study w e r e
reviewed by competent authority consisting of p e r s o n s mentioned i n a footnote t o the front page.
Yet t o be accomplished i s the submission of the conclusions of this paper to the J u d i c i a l Commission of the I n t e r national Committee on Bacteriological Nomenclature f o r
consideration and any action that might be required o r app ropriate
.
History of the Development of Nomenclature of
Organisms of the P L T group
The background t o the initial d i s c o v e r i e s and e a r l y descriptions of the f i r s t named taxa of the P L T group a r e ably
provided by Thygeson ( 1 9 3 4 , 1 9 6 2 ) and Jawetz ( 1 9 6 4 ) , M e y e r
(1953) and Bedson ( 1 9 5 9 ) . The r e a d e r is r e f e r r e d to these
a r t i c l e s f o r details; however, a s u m m a r y of the past nomenc l a t u r a l proposals related to this group and t h e i r rationale
follow s :
Nocard ( 1 8 9 3 ) proposed the name Bacillus psittacosis
f o r the purported etiologic agent of the d i s e a s e p s i t t a c o s i s
(Greek psittakos
p a r r o t ) . The o r g a n i s m he d e s c r i b e d was
probably Salmonella typhimurium which was often isolated
f r o m p a r r o t s concurrently infected with p s i t t a c o s i s , and occasionally f r o m m a n ; hence, he considered i t to be the cause
of psittacosis.
This opinion prevailed until 1930 when a t
l e a s t five physicians and t h e i r colleagues, s e p a r a t e l y and
concurrently , de s c r i be d the f ilt e r able, obligate int r a c ellula r
-
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
SYSTEMATIC
BACTERIOLOGY
231
p a r a s i t e a s s o c i a t e d with psittacosis in p a r r o t s and m a n
(Bedson, W e s t e r n and Simpson, 1930; Lillie, 1930; Coles,
1930; Levinthal, 1930; Krumwiede c t 51. 1930).
In two a r t i c l e s published i n Lancet in F e b r u a r y , 1930,
Bedson, W e s t e r n and Simpson pointed out the filterability of
a n infectious principle i n t i s s u e s f r o m p a r r o t s and f r o m a
m a n with clinical psittacosis and t h e i r f a i l u r e t o i s o l a t e any
o r g a n i s m able t o grow on bacteriological media. T h e s e
authors w e r e able t o reproduce the d i s e a s e i n budgerigars
and chickens but proposed no name f o r t h e i r f i l t e r a b l e agents.
Two months l a t e r , i n a n A p r i l 11, 1930, i s s u e of the U. S.
Public Health R e p o r t s , R. D. Lillie compared the i n t r a c e l l u l a r o r g a n i s m s encountered i n focal lesions i n p a r r o t s and
a human and concluded:
"Such minute i n t r a c e l l u l a r coccoid and rod-shaped
Gram-negative o r g a n i s m s which have not been cultivated
a r e usually designated as Rickettsia, i n which genus i t
would a p p e a r that they should provisionally be included.
The specific name p s i t t a c i was chosen as indicating a
connection with p a r r o t s . The name Rickettsia psittaci
is herewith proposed and the s p e c i e s i s defined as
minute G r a m - ne gative int racellula r co c coid and bipolar
bacilliform bodies of about 0. 2 p t o 0. 3 p i n d i a m e t e r ,
found i n reticulo-endothelial c e l l s , m e s o t h e l i a l c e l l s ,
and l a r g e mononuclear c e l l s of the p a r r o t (probably
Amazon sp.) and i n l a r g e mononuclear cells in m a n ,
a s s o c i a t e d with, but without established relationship
to, p s i t t a c o s i s . I '
Today, m e m b e r s of t h e p r e s e n t genus Rickettsia a r e
readily distinguished f r o m P L T o r g a n i s m s on the b a s i s of
t h e i r antigenicity, pathogenicity, and metabolic patterns.
While t h e r e a r e some s i m i l a r i t i e s i n s i z e and affinity f o r
dyes , the r i c k e t t s i a e f o r m a n a t u r a l group metabolically
distinct f r o m P L T o r g a n i s m s (Bovarnick, 1956; W e i s s , 1964,
1965). Thus, Lillie placed the etiologic agent of psittacosis
i n the previously d e s c r i b e d and named genus Rickettsia.
The name was validly published, but the o r g a n i s m was l a t e r
t r a n s f e r r e d to another genus.
Coles r e p o r t e d i n t h e May 20, 1930 i s s u e of Lancet the
finding of minute bodies in t i s s u e s m e a r s f r o m a chickenand
two m i c e which had been inoculated with infectious m a t e r i a l
f r o m c a s e s of human psittacosis. He observed p a i r e d cocci
0. 6 - 0 . 7 p i n length and 0. 3-0. 4 p in d i a m e t e r and opined:
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
232
INTERNATIONAL JOURNAL
" T o m y m i n d , t h e y v e r y c l o s e l y r e s e m b l e s o m e of
t h e r i c k e t t s i a bodies. I c o m p a r e d t h e m with a s l i d e of
R i c k e t t s i a p r o w a z e k i of typhus f e v e r in t h e l o u s e and
t h e y b o r e a s t r i k i n g s i m i l a r i t y t o the coccoid and p a i r e d
coccoid s t a g e of t h e s e b o d i e s . .
T h e coccoid bodies
a r e s m a l l enough t o p a s s t h e S e i t z f i l t e r s and have been
v e r y definitely found i n t h e f i l t r a t e , a n d t h e s e m a y p r o v e
t o be t h e c a u s a l o r g a n i s m s of t h i s o b s c u r e d i s e a s e .
T h e y m i g h t p r o v i s i o n a l l y be t e r m e d t h e coccoid X
bodies of p s i t t a c o s i s . "
.
Coles did give a n E n g l i s h v e r n a c u l a r n a m e which w a s
quite p r o p e r . Although h i s d e s c r i p t i o n w a s validly published,
h e did not choose t o p r o p o s e a s c i e n t i f i c n a m e .
S i m i l a r independent o b s e r v a t i o n s of the agent of p s i t t a c o s i s w e r e m a d e by W . Levinthal who r e p o r t e d h i s findings
a t the 1 s t I n t e r n a t i o n a l C o n g r e s s of Microbiology i n P a r i s
i n 1930 (published i n 1932). He s u g g e s t e d the n a m e M i c r o b a c t e r i u m m u l t i f o r m e p s i t t a c o s i s b a s e d on h i s c l i n i c a l a n d
m i c r o s copis obs e r v a t i o n s
L e v i n t h a l ' s t r i n o m i a l i s i l l e git i m a t e f o r two r e a s o n s : Code r u l e 24d m a k i n g l a t e r homon y m s unacceptable and Code r u l e 6 which r u l e s out t r i n o mials.
In t h i s c a s e , Levinthal, p e r h a p s unintentionally,
u s e d a g e n e r i c n a m e p r e v i o u s l y validly published by O r l a
J e n s e n i n 1919 f o r the l a c t i c a c i d b a c t e r i a .
Throughout t h e p e r i o d between 1930 and 1938, Bedson and
h i s colleagues continued t o study t h e r e l a t i o n s h i p between
t h e i n t r a c e l l u l a r p a r t i c l e s s e e n i n infectious t i s s u e s f r o m
p s i t t a c o s i s c a s e s a n d the d i s e a s e i n l a b o r a t o r y a n i m a l s . He
w a s t h e f i r s t t o d e s c r i b e the unique d e v e l o p m e n t a l c y c l e ,
i m m u n i t y , a n t i g e n i c composition, and u s e of c o m p l e m e n t
fixation t e s t s f o r d i a g n o s i s of p s i t t a c o s i s .
Bedson s u m m a r i z e d h i s c l a s s i c a l s t u d i e s of p s i t t a c o s i s i n t h e H a r b e n L e c t u r e s of 1958 ( p u b l i s h e d i n 1959). Throughout all t h i s w o r k ,
Bedson m a i n t a i n e d a n e x t r a o r d i n a r y r e s t r a i n t i n connection
with the n o m e n c l a t u r e of t h e s e o r g a n i s m s , p r e f e r r i n g app a r e n t l y , t o await a c c u m u l a t i o n of sufficient evidence t o
w a r r a n t a definitive n o m e n c l a t u r e . It was unfortunate t h a t
he gave no n a m e s t o the o r g a n i s m s he d e s c r i b e d .
N o s u c h h e s i t a n c y w a s exhibited by t h o s e p e r s o n s w o r k ing with t r a c h o m a . In t h e e a r l y t h i r t i e s , t h e i n t r a c e l l u l a r
bodies originally d e s c r i b e d by H a l b e r s t a e d t e r and von P r o w a z e k in 1 9 0 7 w e r e o b s e r v e d a g a i n by a new g e n e r a t i o n of
w o r k e r s and given n a m e s . In 1907, H a l b e r s t a e d t e r and von
P r o w a z e k had p r o p o s e d the n a m e Chlamydozoa ( f r o m G r .
.
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
SYSTEMATIC
BACTERIOLOGY
233
chlamys = cloak and zoa = a n i m a l s ) f o r a taxon coordinate
with p r o t o z o a a n d b a c t e r i a . T h e p u r p o r t e d e t i o l o g i c a g e n t s
of s e v e r a l d i s e a s e s (including t r a c h o m a ) w e r e p l a c e d h e r e
but without s p e c i e s n a m e s o t h e r t h a n v e r n a c u l a r n a m e s .
L a t e r (1907) von P r o w a z e k p r o p o s e d t h e g e n e r i c n a m e
C h l a m y d o z o o n with a s i n g l e s p e c i e s G. b o m b y c i s f o r t h e
a g e n t c a u s i n g t h e "yellow d i s e a s e " of t h e s i l k w o r m . T h i s
i s the t y p e s p e c i e s of t h e g e n u s Chlamydozoon. He i n c l u d e d
t h e d e s c r i p t i o n of the e t i o l o g i c a g e n t of t r a c h o m a but u s e d
only a v e r n a c u l a r d e s i g n a t i o n . T h e m o r e r e c e n t c o n c l u s i o n
t h a t t h e e t i o l o g i c a g e n t of t r a c h o m a b e l o n g s with t h e b a c t e r i a
a n d t h a t t h e yellow d i s e a s e i s c a u s e d by a v i r u s m a k e s ill e g i t i m a t e t h e a l l o c a t i o n of a n y s p e c i e s of b a c t e r i a t o t h e
genus Chlamydozoon.
I n 1933 a n d 1935, B u s a c c a c o m p a r e d t h e t r a c h o m a o r g a n isms with H a l b e r s t a e d t e r a n d von P r o w a z e k ' s d e s c r i p t i o n s .
On t h e b a s i s of m o r p h o l o g i c a n d t i n c t o r i a l s i m i l a r i t i e s of
the t r a c h o m a o r g a n i s m s t o the r i c k e t t s i a e , Busacca p r o p o s e d the n a m e R i c k e t t s i a t r a c h o m a e ( s i c ) . T h i s . n o m e n c l a t u r a l l a p s u s c a l a m i w a s c o r r e c t e d by F o l e y a n d P a r r o t
( 1 9 3 7 ) t o _R. t r a c h o m a t i s . T h e s e l a t t e r a u t h o r s a l s o r e g a r d e d R i c k e t t s i a t r a c h o m a t i s a s s y n o n y m o u s with C h l a m y d o z o o n
trachomatis.
T h e l a t t e r b i n o m i a l w a s u t i l i z e d i n t u r n by
M o s h k o v s k y ( l 9 4 5 ) a s t h e t y p e s p e c i e s of the genus C h l a m y dozoon of h i s p r o p o s e d f a m i l y C h l a m y d o z o a c e a e , a n d a l s o
by R a k e i n 1948 i n B e r g e y ' s 6th E d i t i o n ( T a b l e 1). A s p r e v i o u s l y pointed out by t h e E d i t o r i a l B o a r d of t h e I n t e r n a t i o n a l Bulletin of B a c t e r i o l o g i c a l N o m e n c l a t u r e ( 1955), t h e
s p e c i e s n a m e Chlamydozoon t r a c h o m a t i s w a s illegitimate
a s a n a m e of a s p e c i e s of b a c t e r i a f o r the r e a s o n t h a t C L a m y d o z o o n b o m b y c i s w a s validly p u b l i s h e d a s a n a m e f o r a
v i r u s . T h e family n a m e Chlamydozoaceae w a s a l s o illegitim a t e f o r u s e in bacteriology.
R a k e , i n t h e 7th e d i t i o n of
B e r g e y ' s Manual proposed the family n a m e Chlamydiaceae.
He a l s o p l a c e d t h e a g e n t s of t r a c h o m a i n t h e g e n u s C h l a m y d i a , a n a m e p r o p o s e d by J o n e s , R a k e a n d S t e a r n s (1945).
The specific epithet f o r t h e s e o r g a n i s m s r e m a i n e d t r a c h o m a t i s . L a t e r Zhdanov ( 1 9 5 3 ) a n d L e v a d i t i e t 51. ( 1 964) u s e d
the binary combination Chlamydia t r a c h o m a t i s .
I n 1935, M i y a g a w a a n d h i s c o l l e a g u e s p u b l i s h e d t h e i r f o u r
r e p o r t s on t h e " V i r u s of l y m p h o g r a n u l o m a i n g u i n a l e N i c o l a s ,
F a v r e a n d D u r a n d , " i n w h i c h he d e s c r i b e d t h e o r g a n i s m ' s
m o r p h o l o g y , f i l t e r a b i l i t y , t r a n s m i s s i o n to l a b o r a t o r y a n i m a l s a n d c u l t i v a t a b i l i t y i n t h e c h i c k e n c h o r i o a l l a n t o i c nicnib r a n e . In 1935 t h e F r e n c h p a r a s i t o l o g i s t , E . B r u m p t , \ < s i t e d
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
234
INTERNATIONAL JOURNAL
Miyagawa's l a b o ra t o ry and was shown s om e s l i des of t hes e
organisms.
In apparent appreciation f o r this cour t es y
Brumpt included a footnote i n an a r t i c l e describing a new
rickettsia1 s p e c i e s , ,R. culicis, a proposal f o r a new genus
and type s p e c i e s Miyagawanella lymphogranulomatosis, i n
honor of P r o f e s s o r Miyagawa (Brumpt, 1938). His wor ds
in the M a r c h 1938 i s s u e of Annales de Par as i t ol ogi e in a
footnote t o the 5th paragraph, page 155 (in t r ans l at i on f r o m
the F r e n c h ) a r e :
"(2) The classification of the re pr es ent at i ves of the
family of ri c k e t t s i a e is v e r y difficult to establish; howe v e r , i t a p p e a r s that one can place, provisionally, alongside t h e genus Rickettsia of da Rocha-Lima (1916), [ a
n a m e ] c re a t e d f o r the p a r a s i t e s of world typhus and
which i s synonymous with the genus Dermacentroxenus
Wolbach (1919), the g e n e ra Wolbachia Hertig (1936),
E h r l i c h i a Mochkovski (1937), Ixodisymbiotes n. g.
Brumpt, f o r t h e numerous polymorphic and specific
symbiotes of the ixodides, and Miyagawanella n. g.
Brumpt. I c re a t e d [t h e name f o r ] t h i s last genus f o r
the s p e c i e s ,M. lymphogranulomatosis n. sp., agent of
climatic bubo which P r o f e s s o r Miyagawa showed and
offered t o m e demonstrative p re p a rat i ons i n Tokyo i n
November 1935.
"It p erh a p s will be possible one day t o include among
the Rickettsia (s i c ) the undefined m i cr obes of vaccinia
(Cytoryctes vacciniae G u a rn i e ri 1892), of r abi es
(Neuroryctes hydrophobiae Calkins), a l s o those of t he
B o r r e l i o t a Goodpasteur 1933, the human and ani m al
v a r i o l a s , of mollus cum contagiosum and various ul t r av i r u s e s i n other diseases."
The validity of Brumpt's Miyagawanella is open t o question. He employed the casualness of a footnote t o propose
a monotypic genus which h e failed t o describe. Rule 1 3 of
the Code s t a t e s :
"The name of a genus or of a subgenus i s not
validly published unless it i s accompanied
(a) by a description of the genus o r subgenus; o r . .
i n t h e c a s e of a monotypic new genus based on
a new s p e c i e s , by a combined gener i c and specific
description of one o r m o r e s p eci es included i n
the genus,
.
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
SYSTEMATIC
BACTERIOLOGY
235
(b) by a description of one o r m o r e s p e c i e s o r by
citation of a previous and effectively published
description of one o r m o r e s p e c i e s included i n
the genus. I '
In actuality, Brumpt proposed a n a m e f o r a n o r g a n i s m
whose taxonomic position w a s o b s c u r e t o h i m f o r he could
only place Miyagawanella alongside the genus R i c k e t t s i a
"provisionally," and he suggested that various pox v i r u s e s
and r a b i e s v i r u s be included among the rickettsiae.
Rule 1.2 of the Code indicates that a n a m e of a taxonomic
group i s validly published only i f i t h a s been definitely a c cepted by the author who published it.
In 1945, two attempts w e r e m a d e t o recognize taxonomically the s i m i l a r i t i e s among the o r g a n i s m s causing lymphogranuloma v e n e r e u m , p s i t t a c o s i s , and trachoma. T h e first
w a s by S. D. Moshkovsky of the Institute of M a l a r i a and
Medical P a r a s i t o l o g y in Moscow. He had previously studied
a rickettsia-like agent causing a leucocytosis of guinea pigs
f o r which he established t h e monotypic genus E h r l i c h i a with
canis in 1937. He a l s o s y s t e m i z e d a l a r g e
the s p e c i e s
group of obligate i n t r a c e l l u l a r p a r a s i t e s under t h e n a m e
Chlamydozoa (Table 3). Moshkovsky applied t h i s n a m e t o
the group of o r g a n i s m s suggested by Brumpt (quoted above)
as being generally related: that i s , ( 1 ) r a b i e s v i r u s which
Moshkovsky placed in the genus N e u r o r y c t e s (Calkins),
( 2 ) the B o r r e l i o t a of Goodpasture, the Cytoryctes of G u a r n i e r i , and the Strongyloplasma of Lipschutz in a new family
Cytoryctaceae, ( 3 ) the t r a c h o m a and inclusion conjunctivitis
o r g a n i s m s and the a n i m a l conjunctivitis o r g a n i s m s of Coles
i n a new f a m i l y Chlamydozoaceae, (4) Rickettsia and k r macentroxenus g e n e r a i n t h e family Rickettsiaceae ( P i n k e r ton), ( 5 ) t h e o r g a n i s m s of lymphogranuloma v e n e r e u m ,
m o u s e pneumonia, and leucocytonosis of dogs, cattle, s h e e p
and guinea pigs under the g e n u s E h r l i c h i a Moshkovsky all in
a new family Ehrlichiaceae. L a s t l y , Moshkovsky placed t h e
r e d blood c e l l p a r a s i t e s of the g e n e r a Bartonella, Haemob a r t one lla, G r a h a m e lla, E p e r ythroz oon and Ae gypt iane lla
i n a new family Bartonellaceae. A s far as the inclusion of
r a b i e s among t h e s e o r g a n i s m s i s concerned, Moshkovsky
mistakenly considered the N e g r i bodies observed i n b r a i n
t i s s u e t o be the r a b i e s virus, and since the N e g r i body app e a r e d t o be similar morphologically t o o t h e r "Chlamydozoa," i t was included.
Moshkovsky s e p a r a t e d t h e s e f a m i l i e s on the b a s i s of t h e i r
E.
-
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
236
INTERNATIONAL JOURNAL
T a b l e 3.
M o s h k o v s k y ' s 1945 s e p a r a t i o n of chlamydia1
o r g a n i s m s based on t h e o r i g i n of h o s t c e l l
attacked.
MESODERMOSIS
(Page is)*
Leucocytomonosis
Characteristic localization of
the parasite i n leucocytes
A.
B.
1. Mononuclear leucocytonosis.
Mononuclear and histocytic
c e l l s are infected.
(a)
Dog
Cattle
Sheep
Guinea Pig
(b )
1. Erythrocytonosis. Erythrocytes
and oncoblasts are infected.
Ehrlichia
Ehrlichia
Ehrlichia
Ehrlichia
Aroya fever
Bartonella
bacilliformis
True erythronosis.
are infected.
Only erythrocytes
2.
cani
bovis
ovlna
kurlovi
Mononuc lear h i s tonosi s ;
besides mononuclear c e l l s ,
fixed tissue elements are
infected t o some degree.
Inguinal
Lymphomatosis
Bronchopneumonia
of mice
and r a t s
Psittacosis
2.
Erythrocytonosis (Bartonellanosis).
Characteristic localization of the
agent i n red blood c e l l s
mononuclear are affected by
Ehrlichia
Basic habitat of the agent
Table 3
E. (Miyagawanella)
lymphogranumolatosis
Bartonellanosis
anemia of r a t s
Haembartonella
muris
Melanosis of
Negroes
Orahamella
t alpae
Eperythrozoon
coccoides
Aegyptiosis
Aegyptianella
pullorum
E. (Miyagawanella)
bronchopneumoniae
E. (Miyagawanella)
psittaci
Granulocytic leucocytonosis
(granulocytonosis)
Circulatory granulocytes are infected.
Field cytoecetes
* Moshkovsky,
S. D.
Cytoecetes microti
"The cytoropic agents of infections and the positions of
the r i c k e t t s i a e i n the system of Chlamydozoa" ( i n Russian).
Advances i n Modern
Biology (Uspekhi Sovremennoi Biologii) 19: 1-44 (1945).
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
SYS T EMATIC
BA C T E R I O L O G Y
237
a p p a r e n t p r e d i l e c t i o n f o r i n f e c t i n g c e l l s only of a c e r t a i n
origin.
According to h i m , o r g a n i s m s f r o m s o m e groups
i n v a d e d c e l l s d e r i v e d only f r o m e c t o d e r m , a n d o r g a n i s m s
f r o m o t h e r g r o u p s invaded c e l l s d e r i v e d only f r o m m e s o d e r m ; hence the t e r m s e c t o d e r m o s i s and m e s o d e r m o s i s .
M o s h k o v s k y ' s r a t i o n a l e f o r t h i s w a s contained i n c e r t a i n
s u m m a r y s t a t e m e n t s i n h i s a r t i c l e , "The cytotropic agents
of i n f e c t i o n s a n d t h e p o s i t i o n s of t h e r i c k e t t s i a e i n the s y s t e m of C h l a m y d o z o a " ( i n R u s s i a n ) ,
". . .
7. In p r i n c i p l e , the c y t o t r o p i c C h l a m y d o z o a c a n
be d i f f e r e n t i a t e d i n t o two s u b g r o u p s . T h e f i r s t s u b g r o u p c o n s i s t s of r e l a t e d p a r a s i t e s i n f e c t i n g c e l l s w h i c h
develop exclusively f r o m the outer g e r m i n a l l a y e r
(ectoderm) o r sometimes derived f r o m other layers.
" T h e s e c o n d s u b g r o u p c o n s i s t s of r e l a t e d p a r a s i t e s
infecting c e l l s originally d e r i v e d f r o m the m e s o d e r m .
"In t h e s u b g r o u p of t h e a g e n t s of e c t o d e r m o s e s i n
the s e n s e m e n t i o n e d a b o v e we have s e p a r a t e d t h e following f a m i l i e s :
Neuroryctaceae - localization in n e r v e c e l l s (genus
Neuroryctes)
C y t o r y c t a c e a e - a g e n t s of g e n e r a l i z e d e p i t h e l i o s i s
(genera Cytoryctes, Borreliota) and also agents
of e p i t h e l i o s i s of s k i n ( g e n u s S t r o n g y l o p l a s m a )
C h l a m y d o z o a c e a e - a g e n t s of l o c a l i z e d e p i t h e l j - o s i s
of m u c o u s m e m b r a n e s ( g e n u s C h l a m y d o z o o n )
"In t h e s u b g r o u p of a g e n t s of m e s o d e r m o s i s we
s e p a r a t e t h e following fami l i e s :
1) Rickettsiaceae
c h a r a c t e r i s t i c localization in
e n d o t h e l i u m of v e s s e l s
(genera Rickettsia,
C owdr i a , De rma c e n t r oxenu s )
2 ) E h r l i c h i a c e a e - c h a r a c t e r i s t i c l o c a l i z a t i o n in
l e u c o c y t e s c i r c u l a t i n g i n blood ( g e n e r a E h r l i c h i a ,
Miyagawanella, Cytoecetis)
3 ) Bartonellaceae - c h a r a c t e r i s t i c localization i n
e r y t h r o c y t e s (gene T a B a r t o n e lla, H a e m o b a r t o n e l l a )
-
-
....
T h e a g e n t s of t r a c h o m a l i k e t h e C h l a m y d o z o a
a n d o t h e r a g e n t s t h a t l o c a l i z e i n t h e e p i t h e l i u m of t h e
m u c o u s m e m b r a n e s h o u l d not be r a n k e d with t h e
Rickettsia. Nonetheless, there i s reason to suppose
t h a t t h e y t r a n s f e r by l i c e ; t h e r e f o r e , t h e s e a r c h f o r
p o s i t i v e W e i l - F e l i x r e a c t i o n s s h o u l d be continued. T h e
s e a r c h f o r a n i n t e r m e d i a t e s t a g e between the t r a c h o m a
I'll.
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
238
INTERNATIONAL
JOURNAL
agents of Chlamydozoa and the b a c t e r i a l type, bacillus
Noguchi, o r s i m i l a r bacteria h a s been fruitless."
The validity of Moshkovsky's basis f o r separation of t h e
families in his ''Chlarnydozoa s y s t e m ' ' may be questioned,
f o r c e l l u l a r h a b i t a t m a y be helpful in classification, but does
not d e s e r v e dominance in any system. His classification
r e p r e s e n t s , n e v e r t h e l e s s , the f i r s t attempt t o delineate the
o r g a n i s m s in the o r d e r Rickettsiales beyond the previously
existing Rickettaiaceae and Bartonellaceae of Gieszczykiewicz (1939). It was unfortunate that his t e r m Chlamydozoa
and i t s subdivisions Chlamydozoaceae and Chlamydozoon
had no nomenclatural standing because of Halbe r s t a e d t e r
and von P r o w a z e k ' s p r i o r use of the genus t o name a virus.
F u r t h e r m o r e , Moshkovsky's inclusion of the lymphogranuloma venereum and mouse pneumonia o r g a n i s m s along with
Donatien and L e s t o q u a r d ' s leucocyte p a r a s i t e s of dogs, catt l e , and sheep i n his previously described genus E h r l i c h i a
was a n unfortunate e r r o r .
In this c a s e , E h r l i c h i a canis w a s validly published in
1937 by Moshkovsky f o r the rickettsia-like, rod-shaped
o r g a n i s m s he observed in the monocytes of infected guinea
pigs. In 1945 he placed Donatien and Lestoquard's organisms as well a s the agents of lymphogranuloma venereum,
mouse pneumonia and p s i t t a c o s i s i n the genus E h r l i c h i a
while recognizing Miyagawanella a s a subgenus f o r t h e l a t t e r
t h r e e organisms. Rule 24d applies t o his e r r o n e o u s placement of the LGV-psittacosis o r g a n i s m s i n Ehrlichia; f o r
P L T o r g a n i s m s cannot be considered congeneric with the
original E h r l i c h i a canis.
The l a t t e r agent was readily
t r a n s m i t t e d by t i c k s and no group antigen n o r developmental
cycle s i m i l a r t o that observed i n all of the P L T o r g a n i s m s
h a s been demonstrated f o r ,E. canis.
T h r e e y e a r s p r i o r to $he appearance of Moshkovsky's
classification, the first nonmorphologic evidence that t h e
t r a c h o m a and inclusion conjunctivitis organisms w e r e similar t o psittacosis-lymphogranuloma v e n e r e u m o r g a n i s m s
c a m e f r o m t h e work of Rake, Shaffer and Thygeson (1942)
who demonstrated that all of t h e s e o r g a n i s m s contained a
common group antigen.
Then i n 1945, J o n e s , Rake and S t e a r n s proved the s u s ceptibility of the agent of lymphogranuloma venereum t o
sulfonamide compounds and noted r e p o r t s that other agents
of the P L T group w e r e a l s o susceptible to t h e s e chemicals.
The authors then stated:
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
SYSTEMATIC
BACTERIOLOGY
239
.
In f a c t , the only so-called v i r u s e s whose
susceptibility t o the sulfonamide has been confirmed
a r e m e m b e r s of the lymphogranuloma-trachomap s i t t a c o s i s group of agents (namely, lymphogranuloma
venereum, t r a c h o m a , inclusion b l e n o r r h e a , and m o u s e
pneumonitis). Evidence h a s accumulated s e r v i n g to
s e p a r a t e this group f r o m the t r u e v i r u s e s , analogous
t o the Rickettsiae, with the name Chlamydia. I '
'I..
J o n e s , Rake and S t e a r n s a l s o m a d e an a p p r o p r i a t e r e f e r ence t o a previously published description of the agent of
lymphogranuloma venereum (Rake, McKee, and Shaffer,
1940). The statement quoted above and r e f e r e n c e to a n app r o p r i a t e description of the o r g a n i s m s r e p r e s e n t s a valid
publication of the g e n e r i c name Chlamydia. A footnote on
page 958 of Bergey's Manual of Determinative Bacteriology,
7th edition, 1957, s t a t e s that Chlamydia J o n e s , Rake and
S t e a r n s , 1945, was a nomen nudum without nomenclatural
standing.
Re-examination shows that the g e n e r i c n a m e
Chlamydia was i n reality validly published i n 1945 and was
legitimate when published by Rake i n 1957 with the type
s p e c i e s Chlamydia t r a c h o m a t i s (Busacca) Rake 1957.
L a t e r , Rake defined the o r g a n i s m s i n the f a m i l y c h l a m y dozoaceae Moshkovsky f o r the 6th edition of Bergey's Manual
of Determinative Bacteriology (1948). He recognized t h e
now invalid g e n e r i c name Chlamydozoon H a l b e r s t a e d t e r and
von P r o w a z e k and the generic name Migagawanella Brumpt
but did not accept the g e n e r i c name E h r l i c h i a Moshkovsky.
In the genus Chlamydozoon he included ,C. t r a c h o m a t i s and
C. oculogenitale. In the genus Miyagawanella he included
eight s p e c i e s ; ,M. lymphogranulomatis ( s i c ) Brumpt, ,M.
p s i t t a c i Lillie, 2. bronchopneumoniae Moshkovsky, ,M.
nithosis Rake, M. pneumoniae Rake, ,M. felis Rake, 2.
louisianae Rake, and 2. illinii Rake.
In r e g a r d to the additional new s p e c i e s , Rake commented
in 1953:
-
or-
"It will be noted that eight s p e c i e s a r e listed. The
right of s o m e of ,these, particularly, perhaps, ,M. illinii,
t o be considered as distinct s p e c i e s m a y be questioned.
F u r t h e r investigation m a y well show that t r u e s p e c i e s
do not e x i s t but that the d e s c r i b e d differences a r e only
at the s t r a i n level. Such lack of complete c l a r i t y is,
i n rn,y opinion, no r e a s o n f o r refusing t o undertake
classification a t this time. Such classification should
be r e g a r d e d as a n active undertaking open to change a t
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
240
INTERNATIONAL JOURNAL
any t i m e that new evidence c o m p e l s s u c h a change. It
should indeed s e r v e t o point t o a r e a s of u n c e r t a i n t y ,
and be a n incentive t o f u r t h e r investigation. I '
Rake f u r t h e r pointed out m o r p h o l o g i c , a n t i g e n i c , toxigenic
a n d m o d e of m u l t i p l i c a t i o n d i f f e r e n c e s between P L T o r g a n isms, r i c k e t t s i a e , a n d pox v i r u s e s .
T h i s c o n t r a s t e d with
Moshkovsky's s e p a r a t i o n of t h e s e g r o u p s of a g e n t s on t h e
b a s i s of c y t o t r o p i s m .
T h u s , the b a s i s f o r t h e s e p a r a t i o n of the P L T g r o u p f r o m
t h e r i c k e t t s i a e and f r o m t h e v i r u s e s b e c a m e c l e a r e r , although t h e i r f i n a l e x c l u s i o n f r o m the v i r u s e s on t h e b a s i s of
t h e i r m e t a b o l i c c a p a b i l i t i e s independent of t h e h o s t c e l l w a s
not shown until r e c e n t l y . O r g a n i s m s of t h e P L T g r o u p c a t a bolize glucose a n a e r o b i c a l l y u n d e r highly s p e c i a l i z e d conditions which include the addition of a d e n o s i n e t r i p h o s p h a t e
( A T P ) ( W e i s s , 1965).
The r i c k e t t s i a e , on t h e o t h e r hand,
do not a p p e a r t o u t i l i z e glucose at all, but r e s p i r e v i g o r o u s l y
i n the p r e s e n c e of glutamate and t h e r e a c t i o n r e s u l t s i n a
net gain i n A T P ( B o v a r n i c k a n d S n y d e r , 1949; Bovarnick,
1956). F u r t h e r m o r e , one of t h e r i c k e t t s i a 1 s p e c i e s , 5.
quintana h a s been cultivated on a l i f e l e s s m e d i u m (Vinson
a n d F u l l e r , 1961). That P L T o r g a n i s m s p o s s e s s both t y p e s
of n u c l e i c a c i d s (RNA and DNA), r e p r o d u c e by d i v i s i o n a n d
m e t a b o l i z e independently of host c e l l s is sufficient t o exclude
t h e m f r o m the v i r u s e s a c c o r d i n g t o t h e c r i t e r i a of Lwoff
( 1957).
I n t h e l a t e f o r t i e s a n d e a r l y f i f t i e s , t h r e e R u s s i a n taxonom i s t s p r e s e n t e d t h e i r views of the c l a s s i f i c a t i o n of P L T
o r g a n i s m s . In a 1949 m o n o g r a p h e n t i t l e d "Guide t o t h e Bact e r i a and A c t i n o m y c e t e s " ( i n R u s s i a n ) , N. A . K r a s i l ' n i k o v
r e p e a t e d Moshkovsky's outline f o r t h e Chlamydozoa while
adding s e v e r a l m o r e s p e c i e s ( T a b l e 1). T h i s w o r k added
nothing of s i g n i f i c a n c e t o the c l a s s i f i c a t i o n within t h i s f a m i l y
of o r g a n i s m s , f o r h e m e r e l y included C o l e s ' a n i m a l conj u n c t i v i t i e s s t r a i n s as s p e c i e s u n d e r t h e genus Chlamydozoon
(while i g n o r i n g the genus C o l e s i o t a R a k e ) but included R a k e ' s
new s p e c i f i c e p i t h e t s pneumoniae, f e l i s , l o u i s i a n a e , and
i l l i n i i ( l e a v i n g out o r n i t h o s i s ) t o M o s h k o v s k y ' s genus E r lichia. F u r t h e r m o r e , he p l a c e d C a r p a n o ' s fowl leucocyton o s i s o r g a n i s m a s E h r l i c h i a a v i u m and M o h a m e d ' s f i s h
l e u c o c y t o n o s i s o r g a n i s m s as 5.P i s c e s a l o n g s i d e _E. kurlovi
of Moshkovsky. The l a t t e r two o r g a n i s m s d e s c r i b e d i n 1936
and 1949, r e s p e c t i v e l y , a r e of questionable n a t u r e .
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
SYSTEMATIC
BACTERIOLOGY
241
In 1950, V. L. Ryzhkov of the USSR's A c a d e m y of Medicine, V i r u s I n s t i t u t e i n Moscow published i n the A c a d e m y ' s
j o u r n a l h i s "Study of the s y s t e m a t i c s of v i r a l ' ( i n R u s s i a n ) .
In t h i s brief and i m a g i n a t i v e study, Ryzhkov d e v i s e d f o u r
c l a s s e s f o r all plant, i n s e c t and a n i m a l v i r u s e s : G a m a l e y a e ,
C r y s t a l l o b i o t a e , A r t h r o d o p h i l a e s , and Chlamydozoa.
He
p l a c e d t h e o r g a n i s m s of the P L T g r o u p i n t h e l a s t c l a s s
with t h e following justification:
"IV C l a s s Chlamydozoa ( P r o w a z e k )
"They a r e p a r a s i t e s of a n i m a l s and m a n . They
contain thymonucleic a c i d and lipoids. S o m e t i m e s one
c a n find a m o u n t s of y e a s t nuclei a c i d ( V i r u s group).
L a r g e s t representatives reach 700
in diameter.
D i a m e t e r s a r e often h i g h e r t h a n 200 m t ~ .but r a r e l y l e s s
t h a n 100 m+~.C h a r a c t e r i s t i c a l l y , they a r e highly
s p e c i a l i z e d . Individual v i r u s e s i n f e c t definite s p e c i e s ;
s o m e t i m e s definite v a r i e t i e s . P r o p e r t i e s of v i r u s c a n
be modified by adaptation and p a s s a g e through a s u i t a b l e
host. N a t u r a l s p r e a d i n g is not a s s o c i a t e d with a c a r r i e r .
Wild a n i m a l r e s e r v o i r s a r e r a r e l y e n c o u n t e r e d . When
t h i s d o e s o c c u r , t h e n the v i r u s m a y be t r a n s f e r r e d
d i r e c t l y t o t h e b e a r e r ( t r a n s m i s s i o n of r a b i e s by wolves
and sanguinovorus a n i m a l s ) . V i r u s is widely d i s s e m i n a t e d i n s k i n l e s i o n s and m u c o s a . P a n t r o p i c v i r u s e s
a r e r a r e l y e n c o u n t e r e d . T h i s c l a s s is l e s s m o n o l i t h i c
t h a n p r e v i o u s ones. Many f a m i l i e s a r e concerned."
(page 15)
"In t h i s c l a s s one should d i s t i n g u i s h , m o r e o r l e s s ,
n a t u r a l o r d e r s . We have added t o t h e n u m b e r s of t h i s
c l a s s by including p r e v i o u s l y i n t a c t g r o u p s of v i r u s e s
which a t p r e s e n t a r e not unified i n t h i s g r o u p , and we
have given the n a m e only t o t h e o r d e r , f a m i l y , and
species.
O r d e r Chlamydozoales
T y p i c a l F a m i l y Chlamydozoaceae. P r o b a b l y the
l a r g e s t n a t u r a l l y o c c u r r i n g group. We 11 diff e r e n t i a t e d e l e m e n t a r y bodies. I '
In R y z h k o v ' s t a b l e of c l a s s i f i c a t i o n f o r t h e f a m i l y Chlam y d o z o a c e a e t h a t follows on page 1 7 , a footnote i n d i c a t e s
t h a t "the f a m i l y E h r l i c h i a c e a e Moshkovsky a n d Chlamydoz o a c e a e Moshkovsky have been unified on the advice of R. M.
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
2 42
INTERNATIONAL JOURNAL
Schen." Thus, Ryzhkov placed the e n t i r e P L T group i n the
genus Chlamydozoon and lists the specific epithets without
indicating whether they w e r e newly proposed n a m e s o r p r e viously proposed names of other authors.
ps ittaci
c olumbi
murinus
felis
meningophilus
cricetis
-
hominus
o s t e ophilu s
monocytaris
lymphophilus
opposumi
t r achomiati
c onj un ctiva e
bovi s
oculoge nit a l e
ke rat o conjunctivae
-
-
While Ryzhkov's taxonomic descriptions w e r e e x t r e m e l y
brief, and he used a n illegitimate g e n e r i c name Chlamydozoon Prowazek, h i s unification of Moshkovsky's f a m i l i e s
E h r l i c h i a c e a e and Chlamydozoaceae strengthened the original proposal of J o n e s , Rake and S t e a r n s (1945) that organisms of the P L T group should be placed i n a single genus.
The s a m e y e a r (1950) that Ryzhkov's "Study on s y s t e m a t i c s of v i r u s e s ' ' appeared, V. M. Zhdanov and R. S. Korenblit published a r e p o r t given i n 1949 a t a scientific conference i n Kharkov entitled "Systematics and nomenclature of
v i r u s e s " (in Russian). In this p r e l i m i n a r y description of
t h e i r s y s t e m , Zhdanov and Korenblit proposed a s e r i e s of
n e w n a m e s f o r pre-existing g e n e r a and s p e c i e s in the o r d e r
Rickettsiales; Philip (1956) subsequently pointed out t h e
invalidity of the numerous synonyms proposed bv Zhdanov
and Korenblit. In r e g a r d t o the nomenclature of P L T o r ganisms Zhdanov and Korenblit included the specific epithets
t r a c h o m a t i s Busacca and oculogenitale Moshkovsky i n t h e
genus Chlamydozoon H a l b e r s t a e d t e r and Prowazek 1907.
They a l s o r e j e c t e d Rake's genus Colesiotawhose specific
epithets conjunctivae (Coles) and conjunctivae p;alli ( C o l e s )
w e r e replaced by p e c o r i s (Zhdanov and Korenblit) and pull o r u m (Zhdanov and Korenblit), respectively. F u r t h e r m o r e ,
they proposed the genus name Rickettsiaformis a s a substitute f o r Miyagawanella Brumpt and E h r l i c h i a Moshkovsky.
Sixteen s p e c i e s w e r e placed i n the genus R i c k e t t s i a f o r m i s ;
nine of which w e r e entirely new names f o r various w e l l
known s t r a i n s ; two names w e r e changed f o r m s of previously
suggested n a m e s , and four epithets w e r e changed f o r m s of
previously suggested n a m e s , and f o u r epithets w e r e t h e
s a m e as those proposed by Rake i n Bergey's 6th Edition
Manual ( 1 948) (Table 1).
The extensive synonymy found i n Zhdanov and Korenblit's
-
-
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
SYSTEMATIC
BACTERIOLOGY
243
proposal w a s repeated and extended i n Zhdanov's l a t e r
monograph, "Guide t o Human and Animal Viruses!' (in Russ i a n ) published in 1953. It i s obvious that t h e s e a u t h o r s
c o n s i d e r e d the o r g a n i s m s of the P L T group a s v i r u s e s , a
concept which i s no longer valid. Many of t h e new s p e c i e s
proposed a r e highly questionable, e. g. R. p u l l o r u m Zhdanov
and Korenblit f o r the coccoid f o r m s f r o m chickens studied
by Nelson i n 1936 which a r e now considered t o have been
Mycoplasma gallisepticum. Since the c r i t e r i a f o r speciation within the P L T group have not been stabilized, Zhdanov's
s p e c i e s proposals m a y prove t o have been p r e m a t u r e . In
any c a s e , the genus n a m e R i c k e t t s i a f o r m i s is illegitimate
because it i s a synonym of the previously validly published
g e n e r i c n a m e Chlamydia J o n e s , Rake and S t e a r n s (1945).
In 1952, a t a New York Academy of Sciences conference
on "Nomenclature and Taxonomy of the R i c k e t t s i a l e s , I '
M e y e r (1953) outlined h i s r e a s o n s f o r c o m m e m o r a t i n g S . P.
Bedson i n t h e genus n a m e Bedsonia f o r p s i t t a c o s i s organi s m s and rejecting Brumpt's commemoration of Miyagawa
While m a n y
i n the n a m e Mjyagawanella as inappropriate.
of M e y e r ' s r e a s o n s f o r suggesting the change had m e r i t on
h i s t o r i c a l grounds, the a c t u a l p r o p o s a l d i s r e g a r d e d nomenc l a t u r a l r u l e s of p r i o r i t y ; f o r , the g e n e r i c n a m e Bedsonia
M e y e r (1953) is a junior synonym of Chlamydia Jones, Rake
and S t e a r n s (1945) and t h e r e f o r e i s illegitimate.
Some A m e r i c a n microbiologists have sympathized with
the r e a s o n s f o r M e y e r ' s p r o p o s a l without considering t h e
Code r u l e s and have used the g e n e r i c n a m e Bedsonia and i t s
p l u r a l bedsoniae in d e s c r i b i n g various s t r a i n s of P L T o r ganisms. T h i s h a s effected a d r i f t away f r o m legitimate
bacteriological nomenclature.
In the 7th edition of B e r g e y ' s Manual of d e t e r m i n a t i v e
Bacteriology (1957), Rake included t h e genus Chlamydia f o r
t h e etiologic agents of t r a c h o m a and inclusion conjunctivitis
and the genus Miyagawanella f o r other P L T o r g a n i s m s , but
did not recognize Bedsonia. Under the genus Miyagawanella
h e added four new binary combinations, M. opposumi (Ryzhkov), ,M. &s
(Zhdanov), ,M. bovis (Hork and Baker), and
M . p e c o r i s (Rake). Thus R a k e ' s 1957 l i s t of the P L T o r g a n i s m s did not differ substantially f r o m his 1948 list, other
than recognizing f o u r additional s p e c i e s .
M e y e r ' s Bedsonia w a s d e s c r i b e d in 1964, however, by
Levaditi, R o g e r and Destombes i n t h e i r publication entitled
"Attempts a t a classification of t h e Chlamydiaceae (Rake,
1955) taking into account t h e i r t i s s u e affinities and t h e i r
-
-
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
244
INTERNATIONAL JOURNAL
epidemiology" ( f r o m a u t h o r ' s E n g l i s h s u m m a r y ) .
p r o p o s a l , L e v a d i t i and h i s c o l l e a g u e s d e v i s e d
.
In t h i s
If..
a s i m p l e key utilizing e x p e r i m e n t a l , epidemiologic, and nosologic c h a r a c t e r s w h i c h . .
separates
the f a m i l y of C o l e s i d a e noncultivated i n t h e yolk s a c ,
f r o m t h a t of t h e C h l a m y d i a e , cultivated i n t h e yolk
s a c , and t h e e n d o c e l l u l a r p a r a s i t i s m of which is m o r e
marked;.
' ' ( f r o m a u t h o r s ' English s u m m a r y ) .
.
..
T h e a u t h o r s f u r t h e r c l a r i f y t h e i r r a t i o n a l e by s t a t i n g t h a t :
" T h e f a m i l y of t h e Chlamydidae ( e p i t h e l i a l p a r a s i t e s
of m a n ) d i f f e r s f r o m that of t h e Miyagawellidae ( s i c )
which affect m e s e n c h y m e , a n d i n which the new s u b f a m i l i e s of Miyagawellinae ( s i c ) affecting e s s e n t i a l l y ganglia) and of Bedsoninae ( s i c ) ( e s s e n t i a l l y
s e p t i c e m i c ) m a y s t i l l be distinguished. T h e new
g e n e r a R a k e i a and Bedsonia have been c r e a t e d i n
o r d e r t o e x p l a i n the e s s e n t i a l epidemiologic duality
of t h e Bedsoninae and a s a n homage t o two f o r e i g n
a u t h o r s whose contribution t o t h e knowledge of t h e s e
groups is very important." (authors English s u m m a r y ) .
In e f f e c t , t h e above a u t h o r s a t t e m p t e d t o r e s o l v e t h e "did a c t i c difficulties" ( t o u s e t h e i r t e r m ) by recognizing f o u r
g e n e r a f o r the P L T group, Chlamydia f o r t r a c h o m a and inclusion conjunctivitis o r g a n i s m s , Miyagawanella f o r lympho g r a n u l o m a v e n e r e u m and r e l a t e d o r g a n i s m s , Bedsonia f o r
a v i a n s t r a i n s of the P L T g r o u p , and a new genus R a k e i a
L e v a d i t i , R o g e r and D e s t o m b e s f o r the m a m m a l i a n s t r a i n s .
While t h i s p r o p o s a l a p p e a r s t o soften the "didactic diffic u l t i e s " it c r e a t e s a divisive effect on n o m e n c l a t u r e .
It
p r o m o t e s u n n e c e s s a r y p r o l i f e r a t i o n of g e n e r i c n a m e s , f o r
the t a x o n o m i c value of the d i f f e r e n c e s t h a t L e v a d i t i , R o g e r
and D e s t o m b e s c l a i m s e p ' a r a t e s t h e s e o r g a n i s m s into g e n e r a
( h o s t o r c e l l u l a r p r e f e r e n c e s , epidemiology) d o e s not outweigh the t a x o n o m i c i m p o r t a n c e of the c h a r a c t e r s that unite
t h e m ( c o m m o n m o r p h o l o g y , developmental c y c l e , and g r o u p
antigen).
F u r t h e r m o r e , Levaditi c t 51. have c r e a t e d additional
u n n e c e s s a r y n a m e s of s u b f a m i l i e s and t r i b e s . M o s t of t h e s e
t e r m s i n c o r r e c t l y contain endings u t i l i z e d i n the zoological
code i n s t e a d of endings r e q u i r e d by the b a c t e r i o l o g i c a l code.
In s o m e c a s e s , suffixes w e r e m a n u f a c t u r e d by t h e a u t h o r s
with no known p r e c e d e n t .
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
SYSTEMATIC
BACTERIOLOGY
245
In light of the knowledge of the fundamental s i m i l a r i t i e s
between the o r g a n i s m s of t h e P L T group and the clarification of t h e i r distinction f r o m other o r g a n i s m s ( s u c h as
r i c k e t t s i a e o r v i r u s e s ) , i t is taxonomically and nomenclat u r a l l y c o r r e c t t o place the o r g a n i s m s of t h e P L T group i n
a single genus, Chlamydia J o n e s , Rake and S t e a r n s ( 1945).
By r e a s o n of n o m e n c l a t u r a l p r i o r i t y , the type s p e c i e s i s ,C.
t r a c h o m a t i s ( B u s a c c a ) Rake 1957. Descriptions of t h i s o r g a n i s m a r e found i n publications previously cited, and a r e
reviewed by J a w e t z (1964).
E m e n d e d Description of the Genus Chlamydia,
J o n e s , Rake and S t e a r n s (1945)
S p h e r i c a l o r g a n i s m s , Gram-negative, p a r a s i t e s of the
cytoplasm of host c e l l s , ranging i n s i z e f r o m 200 mp t o
1 0 0 0 mp, and which have a limiting m e m b r a n e r e s e m b l i n g
i n c h e m i c a l composition the c e l l walls of Gram-negative
bacteria. They have a unique developmental cycle following
e n t r y of the s m a l l (200-300 "y.) f o r m of the infectious o r g a n i s m into the cytoplasm of a host cell.
The a r c h i t e c t u r e
of t h e invading o r g a n i s m changes sequentially f r o m l a r g e
(up t o 1000 m p ) homogeneous f o r m s , which multiply by division, to i n t e r m e d i a t e f o r m s with dense c e n t r a l m a s s e s
and s m a l l f o r m s with dense c e n t r a l m a s s e s tightly s u r rounded with outer m e m b r a n e s .
The o r g a n i s m s r e m a i n
s t r u c t u r a l l y intact through all s t a g e s with s o m e d e g r e e of
infectivity, although the infectivity of the l a r g e f o r m s is
v e r y low. An antigenically s i m i l a r carbohydrate lipoprotein
complex is found i n all o r g a n i s m s of the group and i s r e s i s tant t o heating at 100°C f o r 30 minutes. Cell envelopes m a y
contain heat labile, s t r a i n - specific antigens. The o r g a n i s m s
p o s s e s s m e t a b o l i c activities independent of those of the host
cell. The o r g a n i s m s a r e found i n t i s s u e s of n u m e r o u s spec i e s of animals. Pathogenicity v a r i e s considerably. Some
s t r a i n s exhibit m a r k e d cytotropism. All of t h e o r g a n i s m s
a r e influenced by t e t r a c y c l i n e s , s o m e a r e sensitive t o penicillin o r sulfa compounds.
Additional C h a r a c t e r i s t i c s of M e m b e r s of the
Genus Chlamydia
(1) Chemical constituents.
I s o l a t e s examined thus far
contain (a) both RNA and DNA; (b) m u r a m i c acid i n t h e i r
c e l l envelopes along with o t h e r compounds whose g e n e r a l
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
246
INTERNATIONAL JOURNAL
composition r e s e m b l e s that found i n the walls of G r a m negative b a c t e r i a , i. e. , relatively high proportion of lipid,
carbohydrates, and a v a r i e t y of amino a c i d s ; ( c ) a common
group antigen made up of lipo-protein-carbohydrate complex; i n s o m e agents a carbohydrate is p r e s e n t within the
i n t r a c e l l u l a r microcolony which i s differentially stained by
iodine solution o r by periodic acid-Schiff's reagent.
( 2 ) Host range. Numerous i s o l a t e s , especially those of
avian origin, have been shown experimentally t o be able t o
grow, multiply and produce c e l l u l a r and g r o s s pathology i n
a wide range of avian and m a m m a l i a n hosts. Natural i n t e r species t r a n s f e r s occur, but the range and extent of t r a n s f e r s a r e not known.
Arthropods m a y be involved i n t h e
mechanical t r a n s m i s s i o n of c e r t a i n agents between h o s t s ,
but a r e not known to support t h e multiplication of any of t h e
agents. Some agents, such as those that cause t r a c h o m a ,
inclusion conj un ctivi ti s o r 1ymphogr anuloma vene r e u m have
a m a r k e d , n a t u r a l specificity f o r m a n (and f o r p r i m a t e s ,
experimentally) with a f u r t h e r m a r k e d specificity f o r epithelial cells of the conjunctiva o r the genital t r a c t . Cellular
s p e c i f i c i t y a s a basis f o r separation of various o r g a n i s m s of
the group into g e n e r a i s probably artificial.
( 3 ) Metabolism.
At p r e s e n t , propagation of any of t h e
chlamydiae is possible only by allowing the agents t o infect
living t i s s u e cells. However, s e v e r a l i s o l a t e s w e r e shown
to contain enzyme s y s t e m s which a r e not of host origin.
They can synthesize folic acid (Colon, 1960) o r convert host
folic acids to t h e i r own specific f o r m s . They decarboxylate
diaminopimelic acid t o lysine (Moulder, 1963) and, possibly
produce o t h e r c e l l wall components (Moulder, 1964), a n d
degrade t h e i r own p r o t e i n and ribonucleic acid. It was a l s o
shown that under c e r t a i n conditions s e v e r a l s t r a i n s can
catabolize glucose (Weiss, 1964). T h i s reaction r e q u i r e s
added adenosine triphosphate (ATP) and MgSt and is enhanced by added n i c o t i n a q i d e adenine dinucleotide phosphate
The A T P
(NADP) and by high relative concentration of K.'
r e q u i r e m e n t is eliminated by the substitution of glucose-6phosphate f o r glucose.
T h e s e effects a r e obtained with intact cells (Weiss, 1965). Also cell-free e x t r a c t s of purified
chlamydiae contain glucose- 6-phosphate and 6-phosphogluconate dehydrogenase and phosphoglucose i s o m e r a s e (Mould e r , 1965). Synthesis of folic acid i s a l s o suggested on the
basis of the susceptibility of the o r g a n i s m s t o sulfonamides.
On the other hand o r g a n i s m s r e s i s t a n t t o sulfonamides have
been shown t o be uninhibited by folic acid analogues thereby
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
SYSTEMATIC
BACTERIOLOGY
247
suggesting that e s s e n t i a l folic acid p r e c u r s o r s a r e supplied
by the host cell.
(4)Susceptibility to antibiotics. Except f o r experimentally-derived mutants, all of the agents of t h e group t e s t e d
this f a r have been shown to be inhibited i n t h e i r multiplication by tetracyclines. Many a r e inhibited by sulfonamides,
penicillin and other antibiotics. Many isolates a r e r e s i s t a n t
t o streptomycin, tyrothricin, polymixin and neomycin.
(5) Antigens. All i s o l a t e s contain a common antigen
which is heat stable (lOO°C, 30 minutes o r longer) and which
i s destroyed by t r e a t m e n t with periodate. Most i s o l a t e s a l s o
have a specific antigen found i n the c e l l envelope which is
destroyed by heating to 6 0 ° C o r t r e a t e d with any of a l a r g e
number of chemicals.
Other antigenic components with
varying heat sensitivities m a y be p r e s e n t . Many i s o l a t e s
p o s s e s s i n varying amounts a lipoprotein component which
c a u s e s s e v e r e damage to the v a s c u l a r endothelium of s u s ceptible hosts resulting in a "toxic" death. The antigenic
specificity of this component has been useful in grouping
s t r a i n s , but does not regularly p e r m i t the separation of
species.
The genera Colesiota Rake 1948, Colettsia Rake 1957, and
Ricolesia Rake 1957 f o r o r g a n i s m s found in the conjunctiva
of animals a r e r e g a r d e d a s insufficiently c h a r a c t e r i z e d t o
determine t h e i r possible inclusion in the genus Chlamydia.
In s u m m a r y , the t h e s i s i s a n argument f o r the d e s i r ability of recognition of Chlamydia J o n e s , Rake and S t e a r n s ,
1945, a s the name of a genus under which a l l of the s p e c i e s
of the P L T group of b a c t e r i a a r e included, with the type
s p e c i e s being ,C. t r a c h o m a t i s (Busacca) Rake 1957.
ACKNOWLEDGMENT
The author e x p r e s s e s h i s gratitude t o Dr. George Lamb e r t of the National Animal D i s e a s e Laboratory, A m e s ,
Iowa, f o r translating the Russian p a s s a g e s presented i n this
study.
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
248
INTERNATIONAL
JOURNAL
LITERATURE CITED
A d l e r , H . E . and R. Yammamoto. 1956. Studies on chronic
c o r y z a (Nelson) in t h e d o m e s t i c fowl. Cornell Vet.
337-343.
Andrewes, C. 1964. Psittacosis-LymphogranulomaT r a c h o m a Group. Chap. 1 9 & V i r u s e s of V e r t e b r a t e s ,
W i l l i a m s and Wilkins Baltimore. pp. 365- 392.
Bedson, S . P . , G.T. W e s t e r n and S. L. Simpson. 1930. The
aetiology of psittacosis. Lancet c8:235-236.
and
1930. F u r t h e r observations on the
aetiology of psittacosis. Lancet =8:345-346.
1959. T h e H a r b e n L e c t u r e s , 1958. The p s i t t a c o s i s lymphogranuloma group of infective agents. L e c t u r e 1.
The h i s t o r y and c h a r a c t e r s of t h e s e agents. Jour. Roy.
Inst. Pub. Hlth. and H'yg. 22:67-68; L e c t u r e 2. The
ecology of t h e agents of the psittacosis-lymphogranuloma
group. J o u r . Roy. Inst. Pub. Hlth and Hyg. %:99-112;
L e c t u r e 3. The diagnosis, t r e a t m e n t and control of infection of m a n with t h e s e agents. The taxonomic position
of the group. J o u r . Roy. Inst. Pub. Hlth. and Hyg. 2 2 :
131-143.
Bovarnick, M. R. 1956. Phosphorylation accompanying the
oxidation of glutamate by the Madrid E s t r a i n of typhus
rickettsiae. J o u r . Biol. Chem. %0:35.
and J. C. Snyder. 1949. Respiration of typhus rickettsiae. J o u r . Expt. Med. 89:561-565.
Brezina, R. and J. Urvolgyi. 1961. Serological relationships between s o m e v i r u s e s of the bedsonia group and
rickettsiae. Acta virol. 2:255-257.
Brumpt, E . 1938. Rickettsia i n t r a c e l l u l a i r e s t o m a c a l e
(Rickettsia culicis N. Sp.) de Culex fatigans. Ann. de
P a r a s i t o l o g i e e : 1 5 3 - 158.
1949. F a m i l l e des rickettsides. P r e c i s de P a r a s i tologie _1:537,
Busacca, A. 1935. Un g e r m e aux c a r a c t e r e s de r i c k e t t s i e s
(Rickettsia t r a c h o m a e ) dans l e s t i s s u s trachomateux.
Arch. Ophtal., P a r i s 52:567-572.
Coles, A . C. 1930. M i c r o - o r g a n i s m s i n psittacosis.
Lancet 2 1 8 :10 1 1 10 12.
Col6n, J. I. 1960. E n z y m e s f o r formation of c i t r o v o r u m
f a c t o r i n m e m b e r s of the psittacosis group of m i c r o organisms. J o u r . Bact. 3 : 7 4 1 - 7 4 6 .
1962. The role of folic acid i n the m e t a b o l i s m of
m e m b e r s of the psittacosis group of m i c r o o r g a n i s m s .
Ann. N . Y . Acad. Sci. 2:234-245.
46:
.
-.
1
.
-
.
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
SYSTEMATIC
BACTERIOLOGY
249
Gieszcykiewicz, M. 1939. Zagadnienie Systematyki w
Bakt e r iologii- z u r F r a g e de r Bakt e ri en- Sy s t e m a t i k.
Bull. Acad. polon. Sci. S e r i e B. S c i e n c e s N a t u r e l l e s
9- 2 7.
Gordon, F. B. et al. 1962. T h e biology of the t r a c h o m a
agent. Ann. N. Y. Acad. Sci. 28:1-382.
Gordon, M. H. 1930. V i r u s s t u d i e s concerning t h e aetiology
of p s i t t a c o s i s . Lancet 218:1174-1177.
H a l b e r s t a e d t e r , L. and S . von P r o w a z e k . 1907. Ueber
Z e l l e i n s c h l u s s e p a r a s i t a r e r Natur Beim T rachom. Arb.
Gesundhamt. , Berl. 26:44-47.
Huang, K. and E. Weiss. 1965. Metabolic activity of
R i c k e t t s i a quintana. Bact. P r o c . 1965:116.
Huck, R.A. 1964. The c l a s s i f i c a t i o n of v i r u s e s . Vet. Bul.
34:239-253.
J a w e t z , E. 1964. Agents of t r a c h o m a and inclusion conjunctivitis. Ann. Rev. Microbiol. 18:301-334.
J o n e s , H . , G. Rake and B. S t e a r n s . 1945. Studies on
lymphogranuloma v e n e r e u m . 111. The action of the sulf o n e m i d e s on the agent of lymphogranuloma v e n e r e u m .
J o u r . Inf. Dis. 76:55-69.
Ksasil'nikov, N. L. 1949. O r d e r Chlamydozoa P r o w a z e k
1907. In Operdelitel' Bakterien i Aktinomycetov (Guide
t o B a c t e r i a and Actinomycetes). Akad. Nauk SSSR
L e n i n g r a d o r Moscow, U. S. S. R. pp. 730-748.
Krumwiede, C . , M. McGrath and C. Oldenbusch. 1930.
T h e etiology of the d i s e a s e psittacosis. Science 7-l:262263.
Levaditi, J. C . , F. R o g e r and P. Destombes. 1964.
Tenative de c l a s s i f i c a t i o n d e s Chlamydiaceae (Rake,
1955) tenant compte de l e u r s affinites t i s s u l a i r e s e t de
l e u r epidemiologie. Ann. Inst. P a s t e u r
656-662.
Levinthal, W. 1930. Die aetiologie d e r psittakosis. 1 s t
Intern. Congr. Microbiol. P a r i s 1:523-528.
L i l l i e , R. D. 1930. P s i t t a c o s i s - r i c k e t t s i a - l i k e inclusions
i n m a n and i n e x p e r i m e n t a l a n i m a l s . Publ. Hlth. Rep,
Wash. 45:77 3-77 8.
Lwoff, A. 1957. T h e concept of v i r u s . J o u r . Gen. M i c r o biol. 1 7 : 2 3 9- 2 53.
1959. Bacteriolphage a s a m o d e l of host-virus
relationship. Chap. 5 in: The V i r u s e s , edited by F . M .
Burnet and W.M. Stanley. Academic P r e s s , N. Y. Vol.
2~187-201.
M e y e r , K. F. 1940. P s i t t a c o s i s . Auk 2 : 3 3 0 - 3 3 2 .
1953. P s i t t a c o s i s group. Ann. N. Y. Acad. Sci. 5 6 :
545- 556.
(1):
-
107:
.
.
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
250
INTERNATIONAL
JOURNAL
Miyagawa, Y., T. Mitamura, H. Yaoi, N. Ishii, H. Nakaj i m a , J. Okanishi, S . Watanabe, and K. Sato. 1935.
Studies on the v i r u s of lymphogranuloma inguinale Nicolas ,
F a u r e and Durand. F i r s t Report. Jap. J o u r . Exp. Med.
13:1-18.
J
s
?
, and J . Okanishi. 1935. Studies
on t h e v i r u s of lymphogranuloma inguinale Nicolas, F a u r e
and Durand, Second report. E x p e r i m e n t a l findings i n
m o i s e infection. J a p . J o u r . Exp. Med. 2:331-339.
s
?
#
8
1935. Studies on the
v i r u s of lymphogranuloma inguinale Nicolas, F a u r e and
Durand. T h i r d report. Studies on filtration, especially
ultrafiltration of the virus. Jap. J o u r . Exp. Med. 1 3 :
72 3-731.
I
t
3
1
1935. Studies on the
v i r u s of lymphogranuloma inguinale Nicolas, F a u r e and
Durand. F o u r t h r e p o r t . Cultivation of the v i r u s on t h e
chorioallantoic m e m b r a n e of t h e chicken embryo. Jap.
J o u r . Exp. Med. 13:733-750.
Moshkovsky, S . D . 1937. S u r l'existence, chez l e cobaye,
d'une r i c k e t t s i o s e s chronique d e t e r m i n e p a r E h r l i c h i a
(Rickettsia) kurlovi subg. nov., sp. nov. Compt. ren.
SOC. biol. &6:37
9-382.
1945. T h e cytotropic agents of infections and t h e
position of the r i c k e t t s i a e i n the s y s t e m of Chlamydozoa.
Uspekhi Souremennoi Biol. (Advances i n Modern Biology)
19:l-44.
1947. I n : Comments by R e a d e r s . Science =6:62.
Moulder, J. W. 1964. T h e p s i t t a c o s i s group a s bacteria.
J o h n Wiley and Sons, N. Y . , pp. 1-95.
, D. L. Novasel and I. I. E. Tribby. 1963. Diaminopimelic a c i d decarboxylase of the agent of meningopneumonitis. J o u r . Bact. 85:701-706.
9
and
1965. Changes i n m o i s e pneumonitis agent a s s o c i a t e d with development of r e s i s t a n c e t o
chlortet racycline. J our. Bact. 89: 17-22.
, D.L. G r i s s o , and G. J. Cho. 1965. Endogenous
m e t a b o l i s m of protein and ribonucleic acid i n a m e m b e r
of t h e p s i t t a c o s i s group. J o u r . Infect. Dis. %5:254-262.
1966. The relation of t h e p s i t t a c o s i s group (Chlamydiae) t o b a c t e r i a and v i r u s e s . Ann. Rev. Microbiol.
20.
Nelson, J. B. 1936. Studies on uncomplicated Coryza of
d o m e s t i c fowl; coccobacilli f o r m bodies i n b i r d s infected
with C o r y z a of slow onset. J o u r . Exp. Med. 63:515-522.
----
- - - - -.
.
- - - _ I _ -
-.
-.
--
.
-.
-
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
S YSTEMATIC
BAG T E R I 0 L O G . Y
251
Nocard, E. 1893. Conseil. d'hyg. du Depart. de la Seine.
Philip, C. B. 1956. Comments on the classification of the
o r d e r Ri ckett s iale s Canad. Jour M i c r obiol. g:2 6 1-2 70.
Prowazek, S. von. 1907. Chlamydozoa. I. Zuzammenfassende Uebersicht. Arch. Protistenk. 22:248-298.
1907b. Chlamydozoa. II. Gelbsucht d e r Seidenraupen. Arch. P r o t i s t enk. 2 :358- 364.
Rake, G . , C. M. McKee and M. Shaffer. 1940. Agent of
lymphogranuloma venerium i n the yolk-sac of t h e developing chick embryo. P r o c . SOC.Exp. Biol. and Med.
43:332-334.
and H. P. Jones. 1942. Studies on lymphogranuloma
venereum. I. Development of the agent i n the yolk sac of
the chicken embryo. J o u r . Exp. Med. 7-5:323-337.
, M. F. Shaffer and P. Thygeson. 1942. Relationship
of agents of t r a c h o m a and inclusion conjunctivities t o
those of lymphogranuloma-psittacosis group. P r o c . SOC.
Exp. Biol. Med. 49:545-547.
and H. P. Jones. 1944. Studies on lymphogranuloma
venereum. II. The association of specific toxins with
agents of the lympho g r anuloma- ps ittaco s i s group. J our.
Exp. Med. 79:463-485.
and H. Blank. 1950. The relationship of host and
v i r u s in molluscum contagiosium. Jour. Invest. Dermatol. 15:81-93.
1948. F a m i l y . III. Chlamydoxoaceae Moshkovsky.
In: B e r g e y ' s Manual of Determinative Bacteriology, 6th
ed., pp. 1114-1120. Williams and Wilkins, Baltimore,
Md.
1953. The lymphogranuloma-psittacosis group.
Ann. N.Y. Acad. Sci. 56:557-560.
1957. F a m i l y II. Chlamydiaceae Rake F a m . Nov.
In: Bergey's Manual of Determinative Bacteriology, 7th
e d . , pp. 957-968. W i l l i a m s and Wilkins, Baltimore, Md.
Ryzhkov, V. L. 1950. Study on s y s t e m a t i c s of viruses.
Voprosy Meditsinskoi Virusologii Moskau 2:9-19.
Sprockhoff, H. 1953. U b e r s i c h t s r e f e r a t iiber die P s i t t a k o s e
und Ornithose zugleich iiber die s y s t e m a t i s c h e Stellung
d e r E r r e g e r d i e s e r Krankheiten. Dtsch. t i e r a r z t l .
Wschr. 23:256-259.
T e r z i n , A. L. 1958. Psittacosis-ornithosis-mammalian
pneumonitis (POMP) v i r u s e s i n man, m a m m a l s and
birds. J o u r . Hyg., Epidem., Microbiol. and Immunol.
2: 12 9- 141.
.
.
.
-
-
-.
-
.
.
-
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50
252
INTERNATIONAL
JOURNAL
Thygeson, P. 1934. T h e n a t u r e of t h e e l e m e n t a r y and
initial bodies of trachoma. Arch. Ophtal., P a r i s 12:308317.
1962. T r a c h o m a virus: h i s t o r i c a l background and
review of i s o l a t e s . Ann. N. Y. Acad. Sci. 2 : 6 - 1 3 .
Vinson, J. W. and H. S. F u l l e r , 1961. Studies on t r e n c h fever.
I. Propagation of ri-ckettsia-like m i c r o o r g a n i s m s f r o m a
patient’s blood. Pathol. Microbiol. 2 4 (suppl.) 152- 166.
W e i s s , E . , W . F . M y e r s , H. R. D r e s s l e r and H. Chun-Hoon.
1964. Glucose m e t a b o l i s m by m e m b e r s of the p s i t t a c o s i s t r a c h o m a group. Virology 22:551-562.
and H. R. D r e s s l e r . 1965. Adenosine triphosphate
and o t h e r r e q u i r e m e n t s f o r glucose utilization by the
agent of meningopneumonitis. J o u r . Bact. 90:243-253.
Wilner, B.I. 1964. A classification of the m a j o r groups of
human and lower a n i m a l v i r u s e s . Monograph published
by Cutter L a b o r a t o r i e s , Berkeley, California. pp. 1-58.
2nd e d . , 1964.
Zhdanov, V. and R. S. Korenblit. 1950. S y s t e m a t i c s and
nomenclature of v i r u s e s . Zhur. Mikrobiol. Epidemiol.
Immunobiol. 2:40-44. (Report at scientific conference
Ukranian Inst. i m e n i Mechnikov i n Kharkov 11 October
1949).
Zhdanov, V. 1953. Guide t o t h e human and a n i m a l v i r u s e s .
Akad. Med. Nauk. SSSRMoscow, pp. 1-348.
.
Downloaded from www.microbiologyresearch.org by
IP: 78.47.19.138
On: Thu, 29 Sep 2016 17:48:50