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Ten New Species of Legionella DON J INTERNATIONAL JOURNALOF SYSTEMATIC BACTERIOLOGY, Jan. 1985, p. 50-59 Vol. 35, No. 1 0020-7713/85/010050-10$02.00/0 Ten New Species of Legionella DON J. BRENNER,'" ARNOLD G. STEIGERWALT,l GEORGE W. GORMAN,' HAZEL W. WILKINSON,' WILLIAM F. BIBB,l MEREDETH HACKEL,2 RICHARD L. TYNDALL,3 JOYCE CAMPBELL,4 JAMES C. FEELEY,' W. LANIER THACKER,' PETER SKALIY,l WILLIAM T. MARTIN,' BONNIE J. BRAKE,' BARRY S. FIELDS,' HAROLD V. McEACHERN,~AND LINDA K. CORCORAN' Division of Bacterial Diseases, Center for Infectious Diseases, Centers for Disease Control, Atlanta, Georgia 30333'; Pathology Department, University Hospital, University of Michigan, Ann Arbor, Michigan 481 092; Environmental Sciences Division, Department of Zoology, University of Tennessee, Knoxville, Tennessee 379163; and Ofice of Public Health Laboratories and Epidemiology, Department of Social and Health Services, Seattle, Washington 981 044 Ten new Legionella species were characterized on the basis of biochemical reactions, antigens, cellular fatty acids, isoprenoid quinones, and deoxyribonucleic acid relatedness. Nine of the new species were isolated from the environment, and one, Legionella hackeliae, was isolated from a bronchial biopsy specimen obtained from a patient with pneumonia. The species all exhibited the following biochemical reactions typical of the legionellae: growth on buffered cysteine-yeast extract agar, but not on blood agar; growth requirement for cysteine; gram negative; nitrate negative; urease negative; nonfermentative; catalase positive; production of a brown pigment on tyrosine-containing yeast extract agar; liquefaction of gelatin; and motility. Legionella s4iritensis was weakly positive for hydrolysis of hippurate; the other species were hippurate negative. Legionella cherrii, Legionella steigerwaltii, and Legionella parisiensis exhibited bluish white autofluorescence. Legionella rubrilucens and Legionella erythra exhibited red aqtofluorescence. The other species, L. spiritensis, L. hacke liae, Legionella maceachernii, Legionella jamestowniensis, and Legionella santicrucis did not autofluoresce bluish white or red. All species had cellular fatty acid contents qualitatively similar to those of previously described legionellae and had major amounts of ubiquinones with more than 10 isoprene units in the side chains. Each new species was serologically distinct from previously described Legionella species. As determined by the hydroxyapatite method at 60°C, two strains of L. maceachernii were 100% related, and four strains of L. cherrii were 94 to 99% related. The other new species were represented by single strains. The levels of relatedness of the new species to each other and to previously described legionellae ranged from 1 to 67%. L. maceachernii, L. japestowniensis, and L. hackeliae were less than 25% related to other species. L. rubrilucens and L. erythra, and two red-autofluorescing species, were about 60% interrelated. L. spiritensis (a non-au- tofluorescing species) was 34% related to L. rubrilucens. L. santicrucis was 64% related to Legionella sainthelensi. The three bluish white-autofluorescing species, L. parisiensis, L. cherrii, and L. steigerwaltii, were most closely related to other bluish white-autofluorescing species, especially Legionella bozemanii, Legionella dumofli, Legionella gormanii, and "Legionella anisa" (35 to 67%). A total of 221 cases of pneumonia resulting in 34 deaths organisms were studied biochemically, serologically, chem- occurred during an epidemic at the American Legion Con- ically for total cellular fatty acids, and by DNA relatedness. vention in Philadelphia, Pa., in 1976 (22,23). After a massive New species were proposed, as indicated by these data, with investigation of this epidemic, the etiological agent of the a present total of 12 named species. Legionella bozemanii (6, so-called Legionnaires disease was finally isolated by 9, 27) was first isolated in 1959 and Legionella micdadei (27, McDade et al. (36). This organism was shown to be a 28, 48, 50) was first isolated in 1943; both of these species bacterium that was phenotypically unique, whose deoxyribo- have been isolated from patients with pneumonia. L. mic- nucleic acid (DNA) was unrelated to the DNAs of all other dadei has also been isolated from human blood and from species tested (10-12, 45). Therefore, it was classified in a water and is commonly referred to as the Pittsburgh pneu- new genus and species, Legionella pneumophila, in the new monia agent (48). Legionella dumofii was isolated first from family Legionellaceae (10). L. pneumophila was subse- water and later from human lung tissue (9, 33). Legionella quently shown to be a major cause of both pneumonia and an gormanii (18, 41) was isolated from water, but serological acute, self-limiting febrile disease called Pontiac fever (31). evidence implicated it as another agent of Legionnaires The public health significance of Legionnaires disease stim- disease. Legionella longbeachae (37) has only been isolated ulated many intense investigations. It was soon learned that from humans, with strains of this species falling into two L. pneumophila had first been isolated in 1947 (35; E. B. serogroups (3, 37). Legionella jordanis has been implicated Jackson, T. T. Crocker, J. E. Smadel, Bacteriol. Proc., p. in human pneumonia by indirect fluorescent antibody reac- 119, 1952). We now recognize at least 10 serogroups in L. tions with human sera (15) and was recently isolated from pneumophila (2, 4, 49, 38, 39; W. F. Bibb and R. M. human lung tissue (51); it has also been isolated from water McKinney, unpublished data). L. pneurnophila strains were and sewage. Legionella oakridgensis (47) and Legionella isolated-from patients with pneumonia and from the environ- sainthelensi (14) were isolated from water and have not been ment. isolated from or implicated in cases of human pneumonia. Strains that resembled L. pneumophila but differed in one Legionella wadsworthii (19) was isolated from a patient with or more phenotypic characteristics were called Legionella- pneumonia. Legionella feeleii was isolated from an indus- like organisms. Representative strains of Legionella-like trial water source in a factory where an outbreak of Pontiac fever occurred (29); it was not isolated from patients in this outbreak, but serological evidence indicated that L. feeleii * Corresponding author. was the causative agent. L.feeleii was also recently isolated 50 VOL.35, 1985 TEN NEW LEGIONELLA SPECIES 51 TABLE 1. Legionella strains Strain Source Location Method” Isolated by: G+C content (rnol%) L. pneurnophila Lung tissue, human Philadelphia, Guinea pig-egg-+MHIH J. E. McDade and 39(10), 39(4)h Philadelphia lT pneumonia Pa. R. E. Weaver (28 (= ATCC February 1977) 33152T) L. bozemunii Lung tissue, human Key West, Guinea pig-egg-CY E F. M. Bozeman 43(35), 41(13) WIGA~ Fla. (G. A. Hebert) (= ATCC 1957 (25 May 1979) 33 2 17T) L. rnicdudei Blood, human Fort Bragg , Egg-CY E H. Tatlock 44(4), 41 TAT LOCK^ N.C. (G. A. HCbert) (= ATCC 1943 (25 May 1979) 3321gT) L. durnojjii NY-23T Water, cooling tower New York, Guinea pig-egg-CYE G. W. Gorman 41(13), 42 (= ATCC N.Y. (6 October 1978) 33279T) L. gorrnanii LS-13T Soil, creek bank Atlanta, Ga. Guinea pig-egg-CY E G. W. Gorman 41(13), 41 (= ATCC (1 December 1978) 33297T) L. longbeache Transtracheal aspirate, Long Beach, Direct plating on CYE R. Porschen 40 Long Beach 4T human pneumonia (fatal) Calif. (10 April 1980) (= ATCC 33462T) L. jordunis Water, river Bloomington, Guinea pig-egg-CYE G. W. Gorman 45 BL-S40T Ind. (1 September 1978) (= ATCC 33623T) L. oukridgerisis Water, cooling tower Pennsylvania Guinea pig-+CY E R. L. Tyndall, 4347) Oak Ridge loT C. B. Duncan, and (= ATCC E. L. Domingue 33761T) (April 1981) L. wudsworthii Sputum, human pneumonia Los Angeles, Direct plating on P. H. Edelstein 42( 19) 8 1-71 6T Calif. selective BCYE (23 November (= ATCC 1981) 33877T) L. feeleii Water Windsor, AT, direct plating on G. W. Gorman 46(29) WO-44C-C3T Canada BCYE + AB (August 1981) (= ATCC 35072T) L. suinthelensi Water, spring Mount Saint Direct plating on BCYE J. Campbell and 41(14) Mount Saint Helens, S. Eng (April 1981) Helens 4T Wash. (= ATCC 35248T) “L. unisu” Hot water. sink Los Angeles, AT, direct plating on G. W. Gorman 42‘ WA-316-C3T Calif. CY E (22 April 1981) (= ATCC 35292T) L. rnuceuchernii Water, home evaporator- Phoenix, Guinea pig-egg-CY E G. W. Corman 43 PX-1-G2-E2T cooler Ariz. (9 July 1979) (= ATCC 35300T) L. rnaceuchernii Potable water cistern St. Thomas. AT, direct plating on G. W. Gorman 41 sc-73-c2 v.1. CY E (24 April 1982) L. jarnesiowniensis Wet soil Jamestown, Guinea pig-egg-+CY E G. W. Gorman 42 JA-26-Gl-E2* N.Y. (12 December (= ATCC 1979) 35298T) L. rubrilucens Tap water Los Angeles, AT, direct plating on G. W. Gorman 52 WA-270A-C2T Calif. CYE (19 June 1980) (= ATCC 35304T) L. erythru Water, cooling tower Seattle, AT, direct plating on G. W. Gorman 51 SE-32A-C8T Wash. BCYE (19 January 1981) (= ATCC 35303T) L. huckeliue Bronchial biopsy, human Ann Arbor, Direct plating on BCYE M. Hackel 40 Lansing 2T pneumonia Mich. (21 July 1981) (= ATCC 35 2SOT) Continued on following page 52 BRENNER ET AL. INT. J. SYST.BACTERIOL. TABLE 1-Continued G+C content Strain Source Location Method” Isolated by: (mol %) L. spiritensis Water, lake Spirit Lake, Direct plating on BCYE J. Campbell 46 Mount Saint Wash. (23 August 1981) Helens 9T (= ATCC 35249T) L. parisiensis Water, cooling tower Paris, France AT, direct plating on G. W. Gorman 42 PF-209C-C2T CYE + AB (9 September 1981) (= ATCC 35299T) L. cherrii ORWT Water, thermally altered Minnesota Guinea pig-CY E R. L. Tyndall and 40 (= ATCC C. B. Duncan 35252T) (8 January 1982) L. cherrii ORB Water, thermally altered Minnesota Guinea pig+CYE R. L. Tyndall and 40 C. B. Duncan (8 January 1982) L. cherrii ORZ Water, thermally altered Minnesota Guinea pig-CY E R. L. Tyndall and 39 C. B. Duncan (8 January 1982) L. cherrii SC-65-C3 Potable water cistern St.
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