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Histophilus Ovislhaemophilus Somnus,' ' Haemophilus INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Jan. 1986, p. 1-7 Vol. 36, No. 1 0020-771 3 /86/0 10001 -07$02.00/0 Copyright 0 1986, International Union of Microbiological Societies Deoxyribonucleic Acid Relationships of “Histophilus ovislHaemophilus somnus,’ ’ Haemophilus haemoglobinophilus, and “Actinobacillus seminis” K. PIECHULLA,l R. MUTTERS,’ S. BURBACH,l R. KLUSSMEIER,’ S. POHL,2 AND W. MANNHEIM1* Zentrum fur Hygiene und Medizinische Mikrobiologie der Philipps- Universitat, Abteilung Bakteriologie, 0-3550Marburg,‘ and Hygiene-Institut der Ruprecht-Karls-Universitat,0-6900 Heidelberg,2 Federal Republic of Germany Three Australian isolates of “Histophilus ovis,?’ ten strains of “Haemophilus somnus” from North America, Australia, and Europe, and two American strains of “Haemophilus agni” were investigated by the deoxyribonucleic acid (DNA)-DNA hybridization (renaturation) method to determine their genetic interrela- tionships and their levels of relatedness to recognized wembers of the family Pasteurellaceae Pohl 1981. Our results confirmed that “Haemophilus somnus,” “Histophilus ovis,” and one of the “Haemophilus agni” strains studied represent one genetically homogeneous species. This species exhibited up to 41 % DNA relatedness to Haemophilus haemoglobinophilus, whereas only insignificant levels of relatedness or no measurable DNA binding was observed with the type species of the genera Actinobacillus, Haemophilus, and Pasteurella and with Haemophilus aphrophilus, Haemophilus ducreyi, Haemophilus paragallinarum, Haemophilus parainfluenzae, Haemophilus segnis, Pasteurella avium, Pasteurella ureae, and “Actinobucillus seminis. ” On the other hand, one of the “Haemophilus agni” strains studied (Hoerlein strain M650-1343) was included in the species “Acfinobacillus seminis” (DNA binding value, 91%). So far, only low levels of genetic relatedness with “Actinobacillus seminis” and currently recognized members of the family Pasteurellaceae have been detected. The problems of the generic affiliation of the “Histophilus ovis” group, Haemophilus haemoglobinophilus, and “Actinobucillus seminis” and the phenotypic differentiation of these organisms are discussed. The hitherto unrecognized taxa “Histophilus ovis” “Haemophilus somnus,” and ‘Haemophilus agni” strains Roberts 1956 (28), “Haemophilus agni” Kennedy et al. 1958 are genetically related at the species level but are not (lo), “Actinobacillus seminis” Baynes and Simmons 1960 significantly related to “Actinobacillus seminis” and a strain (2), “Haemophilus somnus” Bailie 1969 (W. E. Bailie, of Haemophilus inJIuenzae (32). Thus, “Histophilus ovis” Ph.D. thesis, Kansas State University, Manhattan, 1969), and “Actinobacillus seminis” appear to be two distinct and “Haemophilus somnifer” Miles et al. 1972 (19) contain species of the Pasteurellaceae without generic affiliation. important pathogens that have been isolated from domestic In this paper we present DNA-DNA hybridization data for ruminants in Australia, North America, Europe, and South additional strains of “Histophilus ovis,” “Haemophilus Africa. “Actinobacillus actinoides’ ’ and “Haemophilus somnus,’ ’ “Haemophilus agni,” “Actinobacillus seminis, ” citreus” are probably additional synonyms for at least one of and Haemophilus haemoglobinophilus and reference cul- these taxa (30). Details of the histories of these organisms tures representing additional taxa of the Pasteurellaceae. In have been described elsewhere (3, 9, 12, 30, 32). Although this study we also considered DNA base composition and these bacteria fit in the family Pasteurellaceae Pohl on the genome masses and the significance of some phenotypic basis of their phenotypic properties (17), they were not features for differentiation of the genetic groups established. included in the genera Actinobacillus (23, 29) and Haemo- philus (12, 29). Genetically, strains representing “Haemo- MATERIALS AND METHODS philus somnus,” “Haemophilus agni,” and “Actinobacillus Bacterial strains and growth conditions. The bacterial seminis” were placed in the family Pasteurellaceae on the strains investigated and their origins are listed in Table 1. basis of 16s ribosomal ribonucleic acid-deoxyribonucleic Starting from lyophilized cultures, cloned working cultures acid (DNA) hybridization data (M. Van Houcke, Ph.D. on enriched chocolate agar (see below) were used to inoculate thesis, University of Gent, Gent, Belgium, 1983). However, mass cultures and identification test media. “Haemophilus this study did not discriminate among generic groups of the somnus,” “Haemophilus agni,” and “Histophilus ovis” Pasteurellaceae De Ley, personal communication). (J. strains were grown in tryptic soy broth (Difco Laboratories, Attempts to classify the organisms in question at the Detroit, Mich.) supplemented with 0.4% (wt/vol) yeast species level have been more successful. Workers have extract (Oxoid Ltd., London, United Kingdom), 2.0% presented biochemical, serological, and cytochemical evi- (vol/vol) horse serum (Oxoid), 2 mg of thiamine monophos- dence that bacterial strains labeled “Histophilus ovis,” phate (TMP) per liter or 2 mg of pyrophosphate (Sigma “Haemophilus agni,” and “Haemophilus somnus” are Chemical Co., Munich, Federal Republic of Germany) per highly interrelated and may represent a single taxon which is liter (1, 18), and 0.5 g of cysteine hydrochloride (Roth, antigenically related to “Actinobacillus seminis” and Hue- Karlsruhe, Federal Republic of Germany) per liter (30). All mophilus haemoglobinophilus to some extent, but is not supplements were filter sterilized before use. Precultures related to the type species of the genera Haemophilus and were incubated statically in 1-liter batches at 37°C for 8 to 16 Actinobacillus (30). Recent DNA-DNA hybridization stud- h and then adjusted with filter-sterilized 1 M NaHC03 to pH ies have shown that a collection of “Histophilus ovis,” 7.0 and transferred in 500-ml volumes into 2-liter Fernbach flasks. The cultures were shaken moderately until the early * Corresponding author. stationary phase of growth and harvested as described 1 2 PIECHULLA ET AL. INT. J. SYST.BACTERIOL. TABLE 1. Bacterial strains used in this study and their DNA base compositions ~~ Serial G+C content Taxon (as received) Collection no.“ Other designation(s) and origin no. (mol%)h 1 Actinobacillus actinomyceterncomitans NCTC 9710T‘ P. Holm 277l49-50; human 47.1 2 Actinobacillus equuli NCTC 8529T W. C. Miller PM30753; foal 42.9 3 Actinobacillus lignieresii NCTC 4189T L. Thompson 1; cattle, glands, United States 43.4 4 Actinobacillus lignieresii NCTC 4976 P. H. Martin CM2; human 43.4 5 “Actinobacillus seminis’’ ATCC 15768 G. C. Simmons K3844-C; ovine, epididymitis, Australia 43.7 (2)“ 6 Actinobacillus sp. ATCC 27072T R. F. Ross 192; sow, vaginal discharge, United States 41.9 7 ActinobacilluslPasteurella-like HIM 744-4 M. Bisgaard F283 (taxon 2); White Pekin duck, 39.4 peritonitis, Denmark (24) 8 ActinobacilluslPasteurella-like HIM 797-5 M. Bisgaard 3.3 (taxon 5); guinea pig, throat, Denmark 42.1 (5) 9 HIM 794-718 M. Bisgaard 10.4 (taxon 7); guinea pig, throat, Denmark 42.1 (5) 10 ActinobacilluslPasteurella-like NCTC 11412 M. Bisgaard F151 (taxon 3); White Pekin duck, 39.3 salpingitis, Denmark (24) 11 Haemophilus aegyp t ius ATCC 11116T M. Pittman 180-a; human, conjunctiva, United States 38.9 12 Haernophilus aphrophilus NCTC 5886 0. Khairat PM1; human, endocarditis, United Kingdom 43.5 13 Haernophilus aphrophilus NCTC 5906T 0. Khairat 320; human, endocarditis, United Kingdom 43.6 14 Huemophilus ducreyi CIP 54.2T P. Kirsche X2; human, Viet Nam 38.0 15 Haemophilus ducreyi ATCC 27722 C. Zierdt 1X: human, United States 37.6 16 Haernophilus haemoglobinophilus NCTC 1659T P. Fieldes XIII; dog. prepuce, Denmark 37.9 17 Haemophilus haemoglobinophilus NCTC 8540 K. Zinnemann; greyhound, United Kingdom 37.5 18 Haemophilus influenzae NCTC 4560 H. J. Benstedt RAMC 18; human, United Kingdom 38.8 19 Haemophilus injluenzae NCTC 8143T A. B. Rosher 680; human, sputum, United Kingdom 39.0 20 Haemophilus paraphrophilus-like ATCC 7901 M. Pittman 429; human, United States 42.8 21 Haernophilus paragallinarum ATCC 29545’‘ K.-H. Hinz IPDH 2403; chicken, sinus, Federal 42.2 Republic of Germany 22 Haernophilus parahaemolyticus NCTC 8479T M. Pittman 536; human, pneumonia, United States 41.4 23 Huemophilus parainguenzae biotype I1 HIM 170-1 G. Leidy Bossy no. 7; human, United States 41.5 24 Haernophilus parainfluenzae biotype 1 HIM 793-8 M. Kilian HK128; human, sputum, Demark 41.7 25 Haemophilus parainfluenzae biotype I1 HIM 572-1 W. Mannheim (Marburg) 20677-74; humam, sputum, 41.9 Federal Republic of Germany 26 Haernophilus parasuis NCTC 4557T R. E. Shope 1374; swine, United Kingdom 40.4 27 Haernophilus segnis NCTC 10977T M. Kilian HK316; human, dental plaque, Denmark 45.3 28 “Haemophilus agni” HIM 911-2 E. L. Biberstein 902; ovine, septicemia, United States 37.7 (32) 29 “Haemophilus agni” HIM 494-5/6 A. D. Hoerlein M650-1343; ovine, septicemia, United 41.3 States 30 “Haernophilus somnus” HIM 734-5 L. Corboz 719; bull, semen, Switzerland (6) 37.5 31 “Haernophilus somnus’ ’ HIM 734-4 L. Corboz 606; calf, lung, Switzerland (6) 38.1 32 “Haernophilus somnus” HIM 734-6 L. Corboz 43; bovine, uterus, Switzerland (6) 37.0 33 “Haernophilus somnus” HIM 734-7 L. Corboz 679; calf, joint, Switzerland (6) 38.7 34 “Haemophilus somnus” HIM 734-8 L. Corboz 8025; bovine, brain, Switzerland (6) 37.5 35 “Huernophilus somnus” HIM 738-5 R. F. Ross IVDL 1080; bovine, trachea, United States 38.0 36 “Haemophilus
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