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Phylogeny of Legionellaceae Based on Small-Subunit Ribosomal DNA Sequences and Proposal of Legionella Lytica Comb

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Phylogeny of Legionellaceae Based on Small-Subunit Ribosomal DNA Sequences and Proposal of Legionella Lytica Comb INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Apr. 1996, p. 526-531 Vol. 46, No. 2 0020-7713/96/$04.00+0 Copyright 0 1996, International Union of Microbiological Societies Phylogeny of Legionellaceae Based on Small-Subunit Ribosomal DNA Sequences and Proposal of Legionella lytica comb. nov. for Legionella-Like Amoeba1 Pathogens J. V. HOOKEY,l* N. A. SAUNDERS,l N. K. FRY,2 R. J. BIRTLES,2 AND T. G. HARRISON2 Molecular Biology Unit, Krus Reference Division, and Legionella Reference Unit, Respiratory and Systematic Infection Laboratory, Central Public Health Laboratory, Colindale, London NW9 5HT, United Kingdom The 16s rRNA-encoding gene sequences from strains of the family Legionellaceae, Sarcobium lyticum, and Coxiella burnetii were determined. Phylogenetic relationships revealed that all Legionella spp. were members of a coherent monophyletic family. The blue-white autofluorescent species formed a defined cluster bounded by Legionella bozemanii and Legionella tucsonensis. The strains of Legionella pneumophila subsp. pneumophila and Legionella pneumophila subsp. fraseri shared 99.2% sequence identity. A legionella-like amoeba1 pathogen (LLAP-3) showed 99.4% sequence identity to the obligate intracellular bacterial parasite Sarcobium lyticum. A proposal is made for the transfer of Sarcobium lyticum from the genus Sarcobium to the genus Legionella as Legionella lytica comb. nov. On the basis of serology and phenetic and phylogenetic comparisons, the taxa Legionella erythra and Legionella rubrilucens may be regarded as subspecies. The family Legionellaceae was initially proposed for a single Swank (55). PCR products were sequenced directly with the Tag DyeDeoxy genus (Legionella) and species (Legionella pneumophila) ( 10). Terminator kit (Applied BioSystems) according to the manufacturer’s protocol. The primers used were pA (8 to 20), pC (= pEM, 341 to 361), pD (518 to 536) Currently, there are 39 validly described species that have been and pD- (536 to 518), pH (1542 to 1522 [35,36]), pE4 (1113 to 1130 [32]), and isolated from either clinical or environmental sources or both 16S1425r (19). The sequence reaction mixtures were electrophoresed with the (28). All species so far described are gram-negative rods, 0.3 X Applied BioSystems 373A DNA sequencer. lop6 to 0.9 X m in width and 2 X lop6to 20 X lop6 m Data analysis. Sequences were aligned against highly conserved regions by the Multalin alignment computer program (15). Regions of extreme hypervariability or more in length, and polar flagella may be present (40). The or ambiguity were removed from the alignment. Phylogenetic analyses were legionellae all shared additional phenotypic characters that carried out on 46 strains for 1,345 nucleotides with the PHYLIP 3.52~Phyloge- included absence of growth on blood agar, nitrate not being netic Inference Package (J. Felsenstein, University of Washington) supported on reduced, negative reaction for urease, a nonfermentative me- a SunOS 5.4 workstation at the Human Genome Mapping Program Resource Centre (Cambridge, United Kingdom). The reliability of three nodes was as- tabolism, a requirement for L-cysteine and iron salts for pri- sessed by analyzing multiple data sets (X 100). Unrooted consensus trees were mary isolation on solid media, respiratory ubiquinones with 10 calculated from both parsimony (DNAPARS) and distance methods. Painvise or more isoprene units, and a predominance of branched-chain distances between all sequences were inferred from the Jukes and Cantor (33) cellular fatty acids (5, 6, 34, 52). The moles percent guanine- one-parameter model (all substitutions are assumed to be equally likely) and under the maximum-likelihood (DNAML) criteria, whereby each branch of the plus-cytosine content (mol% G+C) ranges from 36.3 (Legio- phylogenetic tree was tested for statistical significance. Trees were constructed by nella cincinnatiensis [49]) to 52.0 for the type strains of Legio- neighbor joining (NEIGHBOR [41]) and by using the algorithm of Fitch and nella geestiana (16) and Legionella rubrilucens (9). Margoliash (FITCH [21]). A majority-rule consensus tree was computed from Though bacterial species were defined on the basis of DNA- trees derived from multiple data sets (X 100) by the CONSENSE program. Nucleotide sequence accession numbers. The accession numbers of the Legio- DNA hybridization data, the interpretation of low DNA hy- nella nucleotide sequences obtained in this study by automated PCR cycling were bridization values for some members of the genus Legionella as follows: Legionella adelaidensis, 249716; Legionella anisa, 232635; Legionella resulted in a proposal to divide the family Legionellaceae into birminghamensis,249717; Legionella bozernanii, 249718 and 249719; Legionella three genera: Legionella sensu stricto, Tatlockia, and Fluori- brunensis, 232636; Legionella chenii, 249720; L. cincinnatiensis, 249721; Legio- nella dumojii, 232637; Legionella fairfeldensis, 249722; Legionella feeleii, bacter (12, 26). 249740; Legionella gormanii, 232639; L. geestiana, 249723; Legionella gratiana, In the current study, comparative 16s rRNA-encoding gene 249725; Legionella israelensis, 232640; Legionella jamestowniensis, 249726; Le- (rDNA) sequencing analysis was employed to further delineate gionella jordanis, 232667; Legionella lansingensis, 249727; Legionella londiniensis, and refine the phylogeny of the Legionellaceae. 249728; Legionella macheachemii, 232641; Legionella moravica, 249729; Legio- nella nautarum, 249730; Legionella oakndgensis, 232643; Legionella parisiensis, 24973 1; Legionella quateirensis, 249732; Legionella quinlivanii, 249733; L. rubri- MATERIALS AND METHODS lucens, 232643; Legionella sainthelensi, 249734; Legionella santicrucis, 249735; Legionella shakespearei, 249736; Legionella steigenvaltci, 249737; Legionella tuc- Bacterial strains, culture conditions, and DNA preparation. Strains of Legio- sonensis, 232644; Legionella wadsworthii, 249738; Legionella worsliensis, 249739; nella (Table 1) were cultured on BCYE agar (20) at 35°C in a humid chamber for and the isolate “Glasgow” 86135785, 249724. Sequences used for comparison in up to 7 days. Chromosomal DNA was extracted after lysis with guanidium this study and those obtained by the reverse transcriptase method were as isothiocyanate reagent (42). follows: L. bozemanii, M3603 1; Legionella eTthra, M36027; Legionella hackeliae, PCR amplification, purification, and automated PCR-directed cycle sequenc- M36028; Legionella longbeachae, M36029; Legionella micdadei, M36032; Legio- ing of 16s rDNA. Amplification was carried out as previously described (32), and nella pneumophila subsp. pneumophita, M36023; Legionella pneumophila subsp. the ca. 1,450-bp product was purified according to the method of Zhen and fraseri, M36025; Legionella spiritensis, M36030; and the isolate LAP-3, 249741 (19, 25). * Corresponding author. Mailing address: Molecular Biology Unit, RESULTS AND DISCUSSION Virus Reference Division, Central Public Health Laboratory, Colin- dale, London NW9 5HT, United Kingdom. Phone: 44 181 200 4400. The phenetic relationships among Legionella spp. are sum- Fax: 44 181 200 1569. Electronic mail address: [email protected] marized in Table 1. As previously noted, the genus Legionella .uk. formed a coherent phenotypic taxon (28), and yet comparisons 526 TABLE 1. Phcnotypic relationships among Legionella species" Growth on Au tofluores- cence (365- Bromo- tyrosine- G+C Taxon Cata,ase Gelati- Hippu- (3-Lactamasc Oxidase Cellular fatty Isoprenoid content cresol supplc- (EMBL accession no.) activity naseduction pro- ratedrolysis hy- production activity acidsh quinoner BCYE BCYE-L- "Gz; purplc mented ( moI % )" cysteine agar L. grutiurzu NCTC 12388 (249725') + - +- ND - + + + -+ ND L. bozemunii" WIGA sgp 1 NCTC 11368 (M36031g), + - + +(BW) -+ + + -+ -+ ND Mi-15 sgp 1 NCTC 11369 (249719'), sgp 2 NCTC 11976 (249718') L. steigeenualfii NCTC 11991 (249737') + + +(BW) --- Nogrowth + + + a-c,,:,, Q-1O-Q- 13 40 L. wadsworfhii NCTC 11532 (249738') + +- - + + + a-C1,:0 Q-10 ND L. cherrii NCTC 11976 (249720') + + +(BW) -- + + + a-C,,,(), i-C,6:o Q-10-Q-13 40 L. gomanitf NCTC 11401 (232639') + + +(BW) + + + a-C15:o Q-12 ND L. purisiensis NCTC 11983 (249731 ') + + +(BW) ND + + + + a-C,s:o Q- 10-Q- 13 42 L. unisd' NCTC 11974 (232635') + + +(BW) -+ + + + a-C1,:0 Q-10, Q-12 42 L. dumoffifl NCTC 11370 (232637') + + +(BW) -- + + +- a-Cls:o Q-12 ND L. tucsonensisf NCTC 124439 (232644') + + +(BW) ND ND + + + a-C,s,o, n-c,,,, ND 44 L. sainthelend NCTC 11988 (249734') + +- -+ + + + i-Cim Q-11, Q-12 ND L. cincinnutiensid NCTC 12438 (249721') + - +- ND + + + ND i-C,6.0, i-C16,, ND 36.3 L. sanficrucis NCTC 11999 (249735') + - +- ND + + + + i-c16:0 Q-10-Q-13 3s L. longbeachad' NCTC 1 1477 (M3602Y) + - +- -+ + + -+ i-C1,:0 Q-12 ND L. pneumophild subsp. pneumophila NCTC 11192 + - +- -+ + + 4- i-Cl6:,, Q-12 39 (M3602Y), subsp. fruseri NCTC 11233 (M3602Y) L. moruvicu NCTC 12239 (249729') + + ND f + + + "-C1,: I ND 41.5 L. quateirensis NCTC 12370 (249732') + + ND + + + + n-C I h: I Q- 13 39 L. shukespearei NCTC 12829 (249736') + + ND - + + + -+ i-C1,:0 Q-12 45.5 L. worsliensis NCTC 13277 (249739') + + ND + + + + + n-C16:l Q-13 41 L. feeleitf NCTC 11978 (249740') + + -+ + - a-C,,,,, n-C,,:, Q-13 ND L. spiritensis NCTC 11990 (M3603W) + + -+ + + + i-C,,:0 Q-10-Q- 13 46 L. londiniensis NCTC 12374 (249728') + - -+ +- + + a-Cls,o,n-C,,,, Q-11, Q-13 43 L. brunensis NCTC 12240 (232636') + + ND % + + + a-C,S:O ND 40.5 L. jordunis' NCTC 11533 (232667') + + - + + + a-C1,,0 Q-13 ND
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