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Phylogeny of 54 Representative Strains of Species in the Family Pasteurellaceae As Determined by Comparison of 16S Rrna Sequences FLOYD E

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Phylogeny of 54 Representative Strains of Species in the Family Pasteurellaceae As Determined by Comparison of 16S Rrna Sequences FLOYD E JOURNAL OF BACTERIOLOGY, Mar. 1992, p. 2002-2013 Vol. 174, No. 6 0021-9193/92/062002-12$02.00/0 Copyright X) 1992, American Society for Microbiology Phylogeny of 54 Representative Strains of Species in the Family Pasteurellaceae as Determined by Comparison of 16S rRNA Sequences FLOYD E. DEWHIRST,1* BRUCE J. PASTER,2 INGAR OLSEN,3 AND GAYLE J. FRASER1 Departments ofPhannacology1 and Microbiology,2 Forsyth Dental Center, Boston, Massachusetts 02115, and Department ofMicrobiology, Dental Faculty, University of Oslo, Oslo, Norway3 Received 3 September 1991/Accepted 14 January 1992 Virtually complete 16S rRNA sequences were determined for 54 representative strains of species in the family PasteureUlaceae. Of these strains, 15 were Pasteurella, 16 were ActinobaciUlus, and 23 were Haemophilus. A phylogenetic tree was constructed based on sequence similarity, using the Neighbor-Joining method. Fifty-three of the strains fell within four large clusters. The first cluster included the type strains of Haemophilus influenzae, H. aegyptius, H. aphrophilus, H. haemolyticus, H. paraphrophilus, H. segnis, and Actinobacilus actinomycetemcomitans. This cluster also contained A. actinomycetemcomitans FDC Y4, ATCC 29522, ATCC 29523, and ATCC 29524 and H. aphrophilus NCTC 7901. The second cluster included the type strains ofA. seminis and PasteureMa aerogenes and H. somnus OVCG 43826. The third cluster was composed of the type strains ofPasteureUla multocida, P. anatis, P. avium, P. canis, P. dagmatis, P. galinarum, P. langaa, P. stomatis, P. volantium, H. haemoglobinophilus, H. parasuis, H. paracuniculus, H. paragaUlinarum, and A. capsulatus. This cluster also contained PasteureUla species A CCUG 18782, Pasteurella species B CCUG 19974, Haemophilus taxon C CAPM 5111, H. parasuis type 5 Nagasaki, P. volantium (H. parainfluenzae) NCTC 4101, and P. trehalosi NCTC 10624. The fourth cluster included the type strains of Actinobacillus lignieresii, A. equuli, A. pleuropneumoniae, A. suis, A. ureae, H. parahaemolyticus, H. parainfluenzae, H. paraphrohaemolyti- cus, H. ducreyi, and P. haemolytica. This cluster also contained Actinobacilus species strain CCUG 19799 (Bisgaard taxon 11), A. suis ATCC 15557, H. ducreyi ATCC 27722 and HD 35000, Haemophilus minor group strain 202, and H. parainfluenzae ATCC 29242. The type strain of P. pneumotropica branched alone to form a fifth group. The branching of the PasteureUlaceae family tree was quite complex. The four major clusters contained multiple subclusters. The clusters contained both rapidly and slowly evolving strains (indicated by differing numbers of base changes incorporated into the 16S rRNA sequence relative to outgroup organisms). While the results presented a clear picture of the phylogenetic relationships, the complexity of the branching will make division of the family into genera a difficult and somewhat subjective task. We do not suggest any taxonomic changes at this time. The family Pasteurellaceae Pohl 1981 (51) is currently nobacillus. Major advances in understanding the phylogeny composed of species in the genera Pasteurella Trevisan 1887 of the members of the family Pasteurellaceae have come (63), Actinobacillus Brumpt 1910 (14), and Haemophilus from the DNA-DNA hybridization studies by the Marburg Winslow et al. 1917 (65). While only 27 species were group as exemplified by the work of Pohl, Mannheim, recognized within this family in Bergey's Manual ofSystem- Mutters, and colleagues (34, 39, 50, 51) and from rRNA- atic Bacteriology (17, 30, 35, 46), over 70 species or taxa DNA hybridization studies by De Ley et al. (21). These from human, mammalian, avian, and reptilian sources have studies have defined species belonging to sensu stricto been described (4-11, 38, 41, 47, 48). Essentially all these definitions of the genera Pasteurella (39), Haemophilus (15), taxa are listed and discussed in a review by Mutters et al. and Actinobacillus (24, 51). These studies have shown that (40). Their review is particularly important in that it desig- the phylogenetic structure of the Pasteurellaceae is complex nates reference strains for each of the described, but not and that more than three genera are required to accommo- formally recognized, taxa. Overviews of research on the date the vast array of species in this group. However, many family Pasteurellaceae can be found in the proceedings of species have not fallen into defined clusters, and the branch- conferences held in Copenhagen in 1980 (31) and Guelph in ing of genus-level clusters remains unclear. To further clarify 1989 (45) and in the monograph "Pasteurella and Pasteurel- the phylogeny of this complex family, we decided to under- losis" (1). take an exhaustive study involving full 16S rRNA sequenc- The taxonomy of the family Pasteurellaceae as a whole ing of strains the more than and of its component genera has been examined by several representing 70 described methodologies. Major studies based on phenotypic traits species or taxa. Comparison of 16S rRNA sequences has include those on Haemophilus by Kilian (29) and Broom and proved extremely useful for determining phylogenetic rela- Sneath (12) and onActinobacillus and Pasteurella by Sneath tionships among eukaryotic and prokaryotic organisms (66, and Stevens (59). The studies by Sneath suggested an 67). Unlike hybridization studies, it is feasible to use com- overlapping interrelationship between Pasteurella and Acti- plete distance matrices where the similarity of every se- quence to every other sequence is determined (4,900 com- parisons for 70 organisms). Treeing algorithms that correctly account for differing branch lengths are then applied to the * Corresponding author. distance matrix data to produce phylogenetic trees. The 2002 VOL. 174, 1992 PHYLOGENY OF STRAINS OF THE PASTEURELLACEAE FAMILY 2003 present report describes our interim findings for studies tree nodes was also examined by generating 15 trees using 14 performed during the past 3 years in which we obtained full different beta and gamma Proteobacteria species as out- 16S rRNA sequence data for over 50 strains. Within the next groups, or no outgroup. The species used as outgroups are year, we hope to obtain 20 to 30 additional sequences for indicated in Table 1. strains representing the remaining described species or taxa within the family Pasteurellaceae. RESULTS AND DISCUSSION MATERLALS AND METHODS 16S rRNA sequences. Virtually complete 16S rRNA se- quences, except for 50 bases at the 3' end, were determined Bacterial strains, sources, and sequence accession numbers. for 52 of the 54 strains. Within the sequenced region, 98% of The strains sequenced in this study, and reference strains the bases, about 1,450 bases, were unambiguously deter- used for comparison in constructing phylogenetic trees, are mined. For two strains, partial sequences were obtained. described in Table 1. Included in this table are the strain ForA. suis CCM 5586T, 1,155 bases were determined. There numbers, the source of the strains, the GenBank accession was a single base difference, G for A at position 257, number for the 16S rRNA sequences, and the literature compared with A. suis ATCC 15557. For [H.] haemoglobin- sources for reference sequences. In Table 1, and throughout ophilus NCTC 8540, 335 bases were determined. There was this report, square brackets are used to indicate that a a single base difference, U for C at position 176, compared species does not belong to the sensu stricto definition of its with [H.] haemoglobinophilus NCTC 1659T. The sequences given genus (brackets around genus) or that the organism is of 14 representative species, aligned with and numbered misnamed (brackets around whole name). Our use of square relative to Escherichia coli (13), are shown in Fig. 1. The brackets differs from that of De Ley et al. (21). Throughout sequences for the 52 fully sequenced strains are available for the text, names refer to type strains unless a strain number is electronic retrieval from GenBank under the accession num- given. bers listed in Table 1. Bacterial culture conditions. Strains of Actinobacillus and Comparisons with previously published Pasteurella se- Pasteurella were cultured aerobically at 37°C for 24 h in quences. Chuba et al. (19) published short partial 16S rRNA brain heart infusion broth (Difco). Haemophilus strains were sequences (445 bases) for seven members of the family cultured in brain heart infusion broth supplemented with X Pasteurellaceae. We found the following number of discrep- and V factors. H. paragallinarum was grown on GC agar ancies between sequences for the organisms examined in (BBL) at 37°C anaerobically for 24 h. H. paraphrohaemolyti- both studies: A. actinomycetemcomitans, 4; A. equuli, 5; A. cus was grown on GC agar at 37°C aerobically for 24 h. lignieresii, 6; H. aphrophilus, 6; H. influenzae, 8; and P. Haemophilus taxon C, Haemophilus minor group strain 202, multocida, 20. We believe that our sequences are accurate and H. parasuis Nagasaki were cultured aerobically for 6 to based on having rechecked our sequencing gels at the 7 days in PPLO broth (Difco) supplemented with 10% yeast discrepant positions, compared conservation of secondary extract (Difco), 5% rabbit serum (Biologos), 0.1% dextrose, structure, and examined consistency with the 54 Pasteurel- and 0.025% NAD (Sigma). laceae sequences in our data base. Each of the Chuba et al. Isolation and purification of rRNA. RNA was isolated and (19) sequences contains four errors in a region conserved in partially purified by a modification of the procedure of Pace all members of the Pasteurellaceae (406 to 436): a gap versus et al. (43) as previously described (44). G at 419, and gaps versus GUA at 428 to 430. While this 16S rRNA sequencing. rRNA was sequenced by a modified report was in preparation, the sequence for H. ducreyi CIP Sanger dideoxy-chain termination technique in which prim- 542' was determined by polymerase chain reaction amplifi- ers complementary to conserved regions were elongated cation of the 16S rRNA gene (56). There are eight discrep- with avian myeloblastosis virus reverse transcriptase (33). ancies between this sequence and ours as follows: A versus The primers used in this study are given in Table 2.
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