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Home , Actinobacillus, Actinobacillus seminis, Pasteurella

INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Apr. 1990, p. 148-153 Vol. 40, No. 2 0020-7713/90/020148-06$02.00/0 Copyright 0 1990, International Union of Microbiological Societies

Actinobacillus rossii sp. nov., seminis Spa nov. , noma rev., Pastewella bettii sp. nov. , lymphangitidis sp. nova, Pastewella mairi sp. nova,and Pasteurella tvehalosi Spa nova

P. H. A. SNEATH1* AND M. STEVENS2 Department of Microbiology, Leicester University, Leicester LEI 7RH,’ and Public Health Laboratory, Leicester Royal InJirmary, Leicester LEI 5 WW,2England

Evidence from numerical taxonomic analysis and DNA-DNA hybridization supports the proposal of new species in the genera Actinobacillus and Pasteurella. The following new species are proposed: Actinobacillus rossii sp. nov., from the vaginas of postparturient sows; sp. nov., nom. rev., associated with epididymitis of sheep; Pasteurella bettii sp. nov., associated with human Bartholin gland and finger infections; Pasteurella lymphangitidis sp. nov. (the BLG group), which causes bovine lymphangitis; Pasteurella mairi sp. oov., which causes abortion in sows; and Pasteurella trehalosi sp. nov., formerly biovar T of Pasteurella haemolytica, which causes septicemia in older lambs.

A recent numerical taxonomic study of the genera Acti- showed overlap values of less than 1% except for the nobacillus and Pasteurella (46) identified several phena that following pairs: and have not yet been formally named. In this paper we describe (2.4%); P. multocida and (1.3%); P. six of these phena as new species, based on evidence that the canis and P. stomatis (2.2%); Pasteurella aerogenes and groups form statistically distinct phenotypic clusters and Pasteurella mairi (1.1%); and P. aerogenes and Actinobacil- also on evidence from DNA studies. lus lignieresii (1.4%). It should be noted that these analyses indicate the adequacy for diagnosis of the set of tests used in MATERIALS AND METHODS the tables; the distinctness of the taxa based on the very Full details of the materials and methods which we used large number of tests described by us previously (46) is a have been published previously (46). The strains were tested good deal greater. The results of DNA studies (13,28, 34,35) in a wide range of conventional tests, and Gower similarity also support the distinctness of the taxa. coefficients were calculated based on 155 unit characters. There has been considerable disquiet for many years The organisms were clustered by using the unweighted pair about the genera Actinobacillus and Pasteurella and their group method with averages; details of this method are relationship to the genus Haemophilus (24). described in reference 45. Overlap statistics were calculated The generic arrangements within the family Pasteurel- by using the OVERMAT program (44) with 23 phena to laceae are currently undergoing considerable change. Thus, ensure that they were phenotypically distinct. The most Haemophilus pleuropneumoniae and pasteurellae causing diagnostic characteristics of the phena were obtained from porcine necrotic pleuropneumonia have been transferred to the DIACHAR prOgram (42). the genus Actinobacillus (36), Pasteurella ureae is more The salient properties of previously validly published closely related to A. lignieresii than to P. multocida (13), and Actinobacillus and Pasteurella species, together with the 16s rRNA sequences indicate that Actinobacillus actino- properties of the new species, are listed in Tables 1 and 2. mycetemcomitnns is more closely related to Haemophilus The quality of the tables for identification was evaluated by injuenzae than to A. lignieresii (12). In this study we using the OVERMAT program and the MOSTTYP program assigned the new species to the genus Actinobacillus or the (43). For this evaluation the symbols in Tables 1 and 2 were genus Pasteurella according to whether they seem more coded as follows: f, 95%; (+) and +L, 85%; d, +w, dw, closely related, on the basis of presently available evidence, wL, dL, and NT, 50%; (-), 15%; and -, 5%. These values to the type species A. lignieresii or the type species P. are the midpoints of the ranges of the scores in the tables or multocida, although we acknowledge that the generic assign- were coded as 85 or 50% because of gaps or difficulties in ments of the new species are highly tentative and perhaps reading weak and late reactions. dubious. These assignments are used for want of something better to get the species on record. It is increasingly difficult RESULTS AND DISCUSSION to differentiate the genera Actinobacillus, Haemophilus, and Pasteurella (22, 25); if these taxa are merged, it should be The internal evaluation of the diagnostic tables (Tables 1 noted that Pasteurella, as the oldest name and a conserved and 2) was broadly satisfactory. The MOSTTYP program name, would take precedence according to Rule 24b of the showed that the most typical possible strains (hypothetical International Code of Nomenclature of (19,23,39). median organisms) identified correctly with their own taxa We retained P. ureae in Table 2 in its more familiar with a Willcox probability value of more than 0.99, except position (11) rather than transfer it to the genus Actinobacil- for Pasteurella stomatis (0.98) and Pasteurella canis (0.82). lus as recently suggested (32) because we feel that the The OVERMAT program showed no overlap that reached evidence from DNA (32) and phenotypic (46) studies is not the 8.2% level, which indicates continuous variation (i.e., sufficiently compelling in a situation where wholesale rather that two taxa run together phenotypically). All taxon pairs than piecemeal revision is needed. There is evidence that strains named Actinobacillus sem- * Corresponding author. inis are heterogeneous (46,50), and it is likely that more than

148 VOL. 40, 1990 NEW ACTINOBACILLUS AND PASTEURELLA SPECIES 149

TABLE 1. Differential characteristics of the species belonging to the genus Actinobacillus”

0, ._ i 8 6 @ B .U $ -*; ._ Test $u, s .9 8 .Y ;=: .s .\h .@ ::: .s = u, 2 .Y uou .2 2 :s $ % -sE & 2 4 s 2 h Tu i 9 9 * 9 9 i .;, 9 + - d + Oxidase + + (+) + Nitrate reduction + + + + ONPG reactionC + + d - Phosphatase + + + - Ornithine decarboxylase - Indole production - Urease + Esculin hydrolysis + ,L NAD requirement - Growth on MacConkey agaf + Beta-hemolysis (sheep cells) - Fermentatiod NT Gas production from glucosef - Acid production from: L- Arabinose - Arbutin NT Cellobiose + Dulcitol - Galactose + rn-Inositol - Lactose + Maltose + Mannitol + Mannose + Melibiose + Raffinose + Salicin + Sorbitol + Sucrose + Tre halose + + - + D-Xylose + + + - G+C content (mol%, range) 42.4 40.9 41.8-43.2 46.9

a Data from references 5-8, 10, 11, 15, 20, 21, 24, 27-31, 33, 34, 46, and 47. ‘ +, 290% of the strains are positive; (+), 80 to 89% of the strains are positive; d, 21 to 79% of the strains are positive; (-), 11 to 20% of the strains are positive; -, 510% of the strains are positive; w, weak reaction; L, late reaction; NT, not tested. ONPG reaction, Hydrolysis of ortho-nitrophenyl-P-galactopyranoside. Positive according to Piechulla et al. (34) and negative according to Sneath and Stevens (46). Different formulations of this medium may explain discrepancies in the reported results; the results for A. pleurupneurnoniae are for medium supplemented with NAD. f In Hugh-Leifson medium (17) containing glucose, with incubation for 48 h at 37°C. g Positive according to Sneath and Stevens (46) and negative according to Kilian and Frederiksen (21) and Phillips (33). one species is implicated in epididymitis of sheep or that epithet, but we retain it for reasons of stability. Without a strains have been misidentified because of the unusually valid name, this organism may not be recognized if it occurs wide range of guanine-plus-cytosine (G+C) ratios, 37.8 to infrequently. Similarly, Pasteurella Zyrnphangitidis may be 48.8 mol% (16). A possible relationship to “Haemophilus not uncommon if it is looked for. agni” (34) is indicated by a high DNA-DNA pairing value to Differences between biovars A and T of Pasteurella one strain (strain M650-1343) of this species, but interpreta- haemolytica have been noticed for a long time (2,11,40,41), tion is uncertain due to doubt over the status of “H. agni,” and these organisms are distinct on the basis of phenotypic whose name at present has not been validly published, and and DNA data (26, 35, 38, 46). It seems likely that Pas- strain M650-1343 may perhaps have been misidentified. The teurella trehalosi comprises biogroups 2 and 4 of Bisgaard revival ofA. seminis fixes the species on one of the strains of and Mutters (7) and Mutters et al. (26), and P. haernolytica Baynes and Simmons (l),who originally named it. sensu strict0 comprises biogroups 1, 5, 6, 7, and 9, but this Pastewella bettii seems to be a distinctive organism, needs further study. similar to members of the P. ureae complex but less meta- A number of other groups have recently been recognized bolically active. We have been unable to find valid publica- in the genus Pasteurella (4, 7, 8, 22). We have not been able tion of this name before 1980; therefore, it cannot be to identify the new species proposed here with any of these revived, so we proposed P. bettii below as a new species. groups. It is likely that many new species await description. Nor have we been able to trace the origin of the specific However, one group, the SP group, appears to be taxon 22 of + TABLE 2. Differential characteristics of the species belonging to the genus Pusteurellau 0wl

I m e il) .Y CI Test D 3'_ '_4 ii E .U B 9 $ B .Y 'U > .s $ a .Y '_s -T 6 .1 E :- .Y 2 9 @J E 3 g&% .U 5 3Ly E p 2 :s 3 5 B -c 2 CI : : 8 2 e 23 'CI 8J -T 2 as 2 6 2 B 2 % a; a; a; a; a; II; a; a; a; Ga; a; a; a; a; a; a; Catalase +b + +,w d + + + + - + (+) + + + + d Z Oxidase d +,w + - + + + + +,w - + + + + + 5 (+) m Nitrate reduction + + + + + + + + + - + + + + y; ONPG reactionC d + - - - - - d + -d - + - (+) - - + Phosphatase + + + + + + + + + +++ + + - + + + Ornithine decar- d - - - + - - - - - (+I d + - - - - d boxylase Indole production (-) - - - d,w + - - - -- (+I + + ,w + - - - Urease + - - - - + - - - ++- + - - - + - Esculin hydrolysis ------d - +d - - - + d - NT NAD requirement - - d ------+ Growth on Mac- + +,w - d - - - + - dd d d - d + d - Conkey agaP Beta-hemolysis ------(+I - -d - - - + (+) - - (sheep cells) Fermentatione + + + + + + + + +++ + + + + +,L + NT Gas production (+) - - d,w - + ,w ------d - - - - - frolo ~lucosee Acid production from: L-Arabinose (+) ------+ - ++d (-1 - d - - - +,L d NT Arbutin ------(-I NT + - - - - - Cellobiose ------(-I ------d - NT Dulcitol ------(-1 ------Galactose + + +,L - + + + + + +++ + + (+I - NT rn-Inositol d ------d - -d - d - + ,L ; - NT Lactose (-1 +,L - - - - - d +,L - (-) - d - (-) - - d,w Maltose + - - - d + + + - d d (-1 d - (+I + (+) + Mannitol d + - - - - - + + + \+) (+I - - d + + + Mannose + + +,L d + + + (-) + +++ + + - + d NT Melibiose d -f ------+ - (-1 d - + f- NT Raffinose d +,w - - - + ,w (+) d - -- - d - - d - NT Salicin ------(-) - d- - (-) - (-1 d - NT Sorbitol (-1 - - - - - (-) + - d (+) d - - d + (-) d Sucrose + + - - + + + + + d+ + + + + + + NT Trehalose - + + - d + + - - + (-1 d (+) + d + - + D-Xylose + d - (-) - d - - d d - - - d T G+C content 41.8 39.922.3 42.W.7 38.6 37.7-39.8 38.941.5 43.6-43.7 42.3<3.6 43.9-45.3 49.7 43.4 40.M3.9 40.3-42.8 40.443.5 46.8f47.0 42.6 41.2-43.7 43.244.8 (mol%, range) ? m Data from reference 5-8, 10, 11, 15, 20, 21, 24, 27-31, 33, 34, 46, and 47. +, 290% of the strains are positive; (+), 80 to 89% of the strains are positive; d, 21 to 79% of the strains are positive; (-), 11 to 20% of the strains are positive; -, 110% of the strains are positive; w, weak .3 reaction; L, late reaction; NT, not tested. ONPG reaction, Hydrolysis of ortho-nitrophenyl-P-galactopyranoside. g Different formulations of this medium may explain discrepancies in the reported results; the results for P. uviurn and P. vofuntium are for medium supplemented with NAD. z In Hugh-Leifson medium (17) containing glucose, with incubation for 48 h at 37°C. 2! f Positive according to Carter (11) and negative according to Kilian and Frederiksen (21) and Sneath and Stevens (46). g VOL. 40, 1990 NEW ACTINOBACILLUS AND PASTEURELLA SPECIES 151 our previous study (46). The SP group was set up by Pasteurella pneumotropica, A. lignieresii, A. equuli, A. suis, Frederiksen (14) for the organism of Stewart and Letscher Haemophilus injluenzae, and Haemophilus aphrophilus, (48), strain P625 (= D1922), which we did not study, but two (13, 34). of our taxon 22 strains, strains A249 and A250, have since The G+C content of the DNA of the type strain is 43.7 been identified as members of the SP group (M. Bisgaard, mol% (T,n method) (25). personal communication). Therefore, consideration should The type strain is strain NCTC 10851 (= ATCC 15768 = be given to establishing a species based on strain P625, Simmons K3844-C = A51 and A65 = 5) (34, 46). In our because the SP group appears to be distinct on the basis of hands this strain was negative for the tests marked d in Table both phenotypic and DNA data (46, 49). 1, except for late reactions in the tests for ornithine decar- The proposed new species are described below. Properties boxylase and acid production form m-inositol and maltose. that are notable in the genera Actinobacillus and Pasteurella Pasteurella bettii sp. nov. Pasteurella bettii (betti’i. M.L. are listed; fuller descriptions are given in Tables 1 and 2 and gen. n. bettii, of Bett, named for a gentleman named Bett in a previous paper (46). The type strains exhibit the majority [Catalog of Strains, 8th ed., American Type Culture Collec- results shown in Tables 1 and 2 unless otherwise stated; our tion, Rockville, Md., 19681, whose identity has not been methods were generally sensitive, so that most of the results traced). Phenon 13 of Sneath and Stevens (46); “Pasteurella marked d in the tables were positive in our hands. sp. bettii” of Kilian et al. (22), Cells are small nonmotile Actinobacillus rossii sp. nov. Actinobacillus rossii (ross. i’i. bacilli and coccobacilli that are often <1 pm long. Gram M.L. gen. n. rossii, of Ross named after R. F. Ross, who reaction is negative. Endospores are not formed. Growth is with his colleagues isolated the organism [37]). Phenon 17 of aerobic and facultatively anaerobic, mesophilic. Surface Sneath and Stevens (46); group “Ross” of Kilian and colonies grown aerobically on sheep blood agar are round, Frederiksen (21). Cells are small nonmotile bacilli, seldom greyish, semitransparent, about 2 mm in diameter after 48 h coccobacilli, that are often >2 pm long. Gram reaction is at 37T, and without hemolysis but sometimes with greening negative. Endospores are not formed. Growth is aerobic and of the erythrocytes. Notable for fermenting carbohydrates facultatively anaerobic; mesophilic. Surface colonies grown slowly and weakly, for not acidifying galactose, and for aerobically on sheep blood agar are round, greyish, semi- giving negative oxidase and urease reactions (46). Other transparent, and about 2 mm in diameter after 48 h at 37”C, properties are shown in Table 2. sometimes showing weak hemolysis without marked green- Isolated from human Bartholin gland and hu- ing of the erythrocytes. Notable for producing acid from man finger infections (Catalog of Strains, 8th ed., American m-inositol and sorbitol, but not from sucrose, and for reduc- Type Culture Collection). ing Janus green (46). Other properties are shown in Table 1. Phenotypically similar to P. ureae and A. actinomycetem- Isolated from the vaginas of postparturient sows and comitans (46). DNA-DNA pairing values of 20 to 40% have aborted piglets (37, 46). been reported to a number of Pasteurella species and to Serological cross-reactions have been reported with Acti- Haemophilus parainjluenzae (28, 33, but values of less than nobacillus suis, A. lignieresii, , and A. 10% have been reported to P. ureae and species of the genus seminis, and P. haemolytica (37). DNA-DNA pairing values Actinobacillus (13). of about 50% or less to A. lignieresii, A. suis, A. equuli, P. The G+C content of the DNA of the type strain is 38.6 haemolytica sensu stricto, and P. ureae have been reported mol% (7’,nmethod) (28). (13, 35). The type strain is strain NCTC 10535 (= ATCC 23273 = The G+C content of the DNA of the type strain is 41.9 CDC 41-5568 = A99 and A271 = 50) (28, 46). In our hands mol%, as determined by the thermal denaturation (T,) this strain was positive for the tests marked d in Table 2, method (25, 34). except for acid production from maltose. The type strain is strain ATCC 27072 (= NCTC 10801 = Pasteurella lymphangitidis sp. nov. Pasteurella lymphangi- Ross 192 = P624 = A55 and A68) (46). In our hands this tidis (1ymph.ang.it’id.is. M.L. gen. n. lymphangitidis, per- strain was positive for the tests marked d in Table 1, except taining to lymphangitis, inflammation of the lymph nodes). for gas production from glucose and acid production from The BL (bovine lymphangitis) bacterium of Jayaraman and lactose. Sethumadavan (18); phenon 4 of Sneath and Stevens (46). Actinobacillus seminis sp. nov., nom. rev. (ex Baynes and Cells are nonmotile bacilli, with some coccobacilli. Gram Simmons 1960). Actinobacillus seminis (sem’in.is. M.L. gen. reaction is negative. Endospores are not formed. Growth is n. seminis, of semen). Phenon 14 of Sneath and Stevens (46); aerobic and facultatively anaerobic, mesophilic. Surface “Actinobacillus seminis” of Kilian and Frederiksen (21) and colonies grown aerobically on sheep blood agar are round, Phillips (33). Cells are small nonmotile bacilli and coccoba- greyish, semitransparent, about 2.5 mm in diameter after 48 cilli that are often >2 km long. Gram reaction is negative. h at 37”C, and nonhemolytic but sometimes showing green- Endospores are not formed. Growth is aerobic and faculta- ing of the erythrocytes. Notable for not reducing nitrate, in tively anaerobic, mesophilic, often requiring 5% CO, on first being sensitive to azide, for acidifying arbutin, and for giving isolation. Surface colonies grown aerobically on sheep blood a negative oxidase reaction (46). In our hands galactose and agar are round, greyish, semitransparent, about 1 mm in mannose were acidified, although both of these reactions diameter after 48 h at 37”C, and without hemolysis but were recorded as negative by Jayaraman and Sethumadavan sometimes with greening of the erythrocytes. Notable for (18). Other properties are shown in Table 2. slow and weak fermentation of carbohydrates, for producing Isolated from lymphangitis in Bos indicus in Southern no acid from maltose or mannose, and for giving a negative India (18). phosphatase reaction (46). Other properties are shown in Weak serological cross-reactions have been reported with Table 1. A. lignieresii and pseudotuberculosis (18). Pheno- Cause of epididymitis of sheep (1) and isolated from typically, this organism has some weak affinities with mem- semen; may be involved in polyarthritis of sheep (33). bers of the genus Yersinia (46), but is evidently allied to the Phenotypically similar to P. ureae (46), but DNA-DNA Actinobacillus-Pasteurella complex (46). pairing values are less than 25% to P. ureae, P. multocida, DNA-DNA pairing tests show low values (less than 30%) 152 SNEATH AND STEVENS INT. J. SYST.BACTERIOL. to P. multocida, P. pneumotropica, P. ureae, A. lignieresii, This organism is phenotypically similar to P. haemolytica, A. equuli, and A. suis (13, 28). In our hands this organism P. pneumotropica, Pasteurella gallinarum, and P. multocida was variable for the tests marked d in Table 2. (46) and shows low DNA-DNA pairing values (15 to 35%) to The G+C content of the DNA of the type strain is 49.7 P. haemolytica, P. gallinarum, P. ureae, and P. multocida mol% (T,n method) (28). (3, 28, 35). The type strain is strain NCTC 10547 (= Jayaraman strain P. trehalosi exhibits a level of pairing of about 62% to I = A82 = 71) (28, 46). In our hands this strain was negative Pasteurella testudinis (26, 28). for the tests marked d in Table 2, except for late reactions in The G+C content of the DNA of one strain of biovar T, the tests for acid production from maltose and salicin. serovar 3/T15 (9), strain NCTC 10624, is 42.6 mol% (T,n Pasteurella mairi sp. nov. Pasteurella mairi (mair’i. M.L. method) (26, 28). gen. n. mairi, of Mair, named after N. S. Mair, who isolated The type strain is strain NCTC 10370 (= SllO = ATCC the organism). Phenon 5 of Sneath and Stevens (46); Pas- 29703 = A92 = serovar 3/T15) (9, 46). In our hands this teurella sp. strain “Mair” of Kilian et al. (22). Cells are small strain was positive for the tests marked d in Table 1, except nonmotile bacilli and coccobacilli. Gram reaction is nega- that inositol was acidified late. tive. Endospores are not formed. Growth is aerobic and facultatively anaerobic, mesophilic. Surface colonies grown ACKNOWLEDGMENTS aerobically on sheep blood agar are round, greyish, semi- This work was supported by project grants from the Medical transparent, and about 3 mm in diameter after 48 h at 37°C; Research Council. they usually have a narrow surrounding zone of hemolysis, We thank P. A. Pel1 for technical assistance and M. J. Sackin for occasionally with greening of the erythrocytes. Notable for help with computing. being sensitive to malachite green and 1% Teepol and for usually giving a positive ornithine decarboxylase reaction; LITERATURE CITED growth on DNase agar (catalog no. CM321; Oxoid, Ltd., 1. Baynes, I. D., and G. C. Simmons. 1960. Ovine epididymitis London, England) shows a characteristic orange fluores- caused by Actinobacilfus seminis n. sp. Aust. Vet. J. 36: cence (46). Other properties are shown in Table 2. 454-459. 2. Biberstein, E. L. 1978. Biotyping and serotyping of Pasteurella This organism has been isolated from abortion in sows and haemofytica, p. 253-269. In T. Bergan and J. R. Norris (ed.), septic infections in piglets; it may occur in other animals Methods in microbiology, vol. 10. Academic Press, Inc. (Lon- (46). It is phenotypically similar to P. haemolytica sensu don), Ltd., London. stricto and A. lignieresii (46). DNA-DNA pairing tests show 3. Biberstein, E. L., and C. K. Francis. 1968. Nucleic acid homol- values of 30 to 50% to some strains of P. aerogenes and P. ogies between the A and T types of Pasteurella haemolytica. J. pneumotropica, but values less than 25% to P. multocida, Med. Microbiol. 1:105-198. Pasteurella volantium, and P. ureae (28, 35). 4. Bisgaard, M. 1984. Comparative investigations of Pasteurella The G+C content of the DNA of the type strain is 43.4 haemolytica sensu stricto and so-called P. haemofytica isolated mol% (T, method) (28). from different pathological lesions in pigs. Acta Pathol. Micro- biol. Immunol. Scand. Sect. B 92:201-207. The type strain is strain dCTC 10699 (= LPHL 5143170 = 5. Bisgaard, M. 1986. Actinobacilfus muris sp. nov. isolated from D1187 = A10 = 68) (28, 46). In our hands this strain was mice. Acta Pathol. Microbiol. Immunol. Scand. Sect. B 94:1-8. negative for the tests marked d in Table 1, except for 6. Bisgaard, M., and E. Falsen. 1986. Reinvestigation and reclas- hemolysis and acid production from m-inositol. sification of a collection of 56 human isolates of Pasteuref- Pasteurella trehalosi sp. nov. Pasteurella trehalosi (tre. laceae. Acta Pathol. Microbiol. Immunol. Sect. B 94:215-222. hal.os’i. M.L. gen. n. trehalosi, pertaining to trehalosum 7. Bisgaard, M., and R. Mutters. 1986. A new facultatively anaer- [trehalose]). P. haemolytica group T, which was distin- obic gram-negative fermentative rod obtained from different guished by Smith (40, 41) from P. haemolytica sensu stricto pathological lesions in poultry and tentatively designated as (which is group A, to which type strain NCTC 9380 of P. taxon 14. Avian Pathol. 15117-127. 8. Bisgaard, M., and R. Mutters. 1986. Characterization of some haemolytica belongs); phenon 9 of Sneath and Stevens (46); previously unclassified “Pasteurella” spp. obtained from the P. haemolytica T of Kilian and Frederiksen (21); P. hae- oral cavity of dogs and cats and description of a new species molytica biovar T of Carter (11). Cells are small nonmotile tentatively classified with the family Pohl 1981 rods and coccobacilli. Gram reaction is negative. Endos- and provisionally called taxon 16. Acta Pathol. Microbiol. pores are not formed. Growth is aerobic and facultatively Immunol. Scand. Sect. B 94:177-184. anaerobic, mesophilic. Surface colonies grown aerobically 9. Bisgaard, M., and R. Mutters. 1986. Reinvestigation of selected on sheep blood agar are round, greyish, semitransparent, bovine and ovine strains previously classified as Pasteurella and about 2.5 mm in diameter after 48 h at 37°C; they usually haernolytica and description of some new taxa within the have a pronounced zone of hemolysis (often double) and Pasteurella haernolytica complex. Acta Pathol. Microbiol. Im- munol. Scand. Sect. B 94:185-193. occasionally produce some greening of the erythrocytes. 10. Bisgaard, M., K. Piechulla, Y.-T. Ying, W. Frederiksen, and W. Notable for giving a weak or negative reaction for catalase Mannheim. 1984. Prevalence of organisms described as Actino- and a negative reaction for urease, in producing acid from bacillus suis or haemolytic Actinobacilfus equuli in the oral sorbitol and trehalose but not from galactoce, and for often cavity of horses: comparative investigations of strains obtained showing delayed fermentation in Hugh-Leifson (17) medium and porcine strains of A. suis senso stricto. Acta Pathol. (46). This organism is distinguished from P. haemolytica Microbiol. Immunol. Scand. Sect. B 92:291-298. sensu stricto by fermenting trehalose but not L-( +)-arab- 11. Carter, G. R. 1984. Genus I. Pusteurella Trevisan 1887, 94AL, hose and usually not galactose or D-(+)-xylose and by being Nom. cons. Opin. 13, Jud. Comm. 1954, 153, p. 552-557. In relatively more resistant to penicillin (2, 11). Other proper- N. R. Krieg and J. G. Holt (ed.), Bergey’s manual of systematic ties are shown in Table 2. bacteriology, vol. 1. The Williams & Wilkins Co., Baltimore. 12. Chuba, P. J., R. Bock, G. Graf, T. Adam, and U. Gobel. 1988. Associated with septicemia in older lambs, unlike P. Comparison of 16s rRNA sequences from the family Pasteuref- haemolytica sensu stricto, which is associated with pneumo- fuceae: phylogenetic relatedness by cluster analysis. J. Gen. nia in cattle and sheep and septicemia in newborn lambs (11, Microbiol. 134:1923-1930. 40, 41). 13. Escande, F., F. Grimont, P. A. D. Grimont, and H. Bercovier. VOL. 40, 1990 NEW ACTINOBACILLUS AND PASTEURELLA SPECIES 153

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