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