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Listeria Ivanovii Subsp. Londoniensis Subsp Nova PATRICK BOERLIN,L JOCELYNE ROCOURT,* FRANCINE GRIMONT,3 PATRICK A

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Listeria Ivanovii Subsp. Londoniensis Subsp Nova PATRICK BOERLIN,L JOCELYNE ROCOURT,* FRANCINE GRIMONT,3 PATRICK A INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Jan. 1992, p. 69-73 Vol. 42, No. I 0020-7713/92/010069-05$02.00/0 Copyright 0 1992, International Union of Microbiological Societies Listeria ivanovii subsp. londoniensis subsp nova PATRICK BOERLIN,l JOCELYNE ROCOURT,* FRANCINE GRIMONT,3 PATRICK A. D. GRIMONT,3 CHRISTINE JACQUET,* AND JEAN-CLAUDE PIFFARETTIl" Istituto Cantonale Batteriologico, Via Ospedale 6, 6904 Lugano, Switzerland, and Unit&d'Ecologie Bacte'rienne, Centre National de Re'firence pour la Lysotypie et le Typage Mole'culaire de Listeria and WHO Collaborating Center for Foodborne Listeriosis2 and Unite' des Ente'robacte'ries, Institut National de la Sante' et de la Recherche Me'dicale, Unit&INSERM 199,3 Institut Pasteur, 75724 Paris Cedex 15, France An analysis of 23 Listeria ivunovii strains in which we used multilocus enzyme electrophoresis at 18 enzyme loci showed that this bacterial species could be divided into two main genomic groups. The results of DNA-DNA hybridizations and rRNA gene restriction patterns confirmed this finding. The DNA homology data suggested that the two genomic groups represent two subspecies, L. ivunovii subsp. ivanovii and L. ivanovii subsp. londoniensis subsp. nov. The two subspecies can be distinguished biochemically on the basis of the ability to ferment ribose and N-acetyl-P-D-mannosamine.The type strain of L. ivanovii subsp. londoniensis is strain CLIP 12229 (=CIP 103466). Of the seven recognized Listeria species, only Listeria MATERIALS AND METHODS monocytogenes and Listeria ivanovii are pathogenic (18). Both of these organisms have been isolated from patients In this study we used 3 L. monocytogenes strains, 2 with clinical symptoms, healthy carriers, and the environ- Listeria innocua strains, 2 Listeria seeligeri strains, 2 Lis- ment, but L. ivanovii (formerly called L. monocytogenes teria welshimeri strains, 2 Listeria grayi strains, 2 Listeria serovar 5) has been isolated less frequently than L. mono- murrayi strains, and 23 L. ivanovii strains (Table 1). All of cytogenes (22, 26, 29). L. ivanovii causes mainly abortion in these strains were registered in the Listeria Collection of the sheep (4, 9, 10, 11, 15); more rarely, it causes diseases in Pasteur Institute (CLIP), Paris, France, or in the Special bovines or in humans (21, 26). All L. ivanovii strains belong Listeria Culture Collection (SLCC), Wiirzburg, Germany. to serovar 5, and reciprocally, all serovar 5 strains are The methods which we used for species identification have members of L. ivanovii. These organisms are members of the been described elsewhere (21). When needed, serotyping of only species in the genus Listeria which gives a positive the strains was kindly performed by workers at the Swiss CAMP reaction with Rhodococcus equi and a negative National Listeria Reference Center, Lausanne, Switzerland, CAMP reaction with Staphylococcus aureus (24). They who used the reference method (23). produce a particularly wide zone of hemolysis on sheep MEE. Lysate preparation, electrophoresis, and enzyme blood agar and produce acid from xylose but not from selective staining were done as described by Selander et al. D-mannitol, L-rhamnose, and a-methyl-D-mannoside (25). (27). Electrophoresis preparations for aconitase, alanine Because of these characteristics, L. ivanovii strains can be dehydrogenase, glutamic-oxalacetic transaminase, nucleo- easily distinguished from strains of the other Listeria spe- side phosphorylase, L-phenylalanyl-L-leucine peptidase, and cies. 6-phosphogluconate dehydrogenase were run in buffer sys- From a taxonomic point of view, Ivanov suggested that L. tem A (Tris citrate, pH 8.0). Electrophoresis preparations monocytogenes serovar 5 should be separated as a distinct for NADP-dependent glutamate dehydrogenase, glucose-6- species from L. rnonocytogenes (11). In 1982, Seeliger et al. phosphate dehydrogenase, lactate dehydrogenase, phospho- also recommended that serovar 5 should be considered a glucose isomerase, and mannose phosphate isomerase were taxon that is distinct from L. monocytogenes (26). On the run in buffer system B (Tris citrate, pH 6.7). Electrophoresis basis of its phenotypic characteristics and the results of a preparations for acid phosphatase, adenylate kinase, cata- DNA homology study (20), the species L. ivanovii was lase, fumarase, NAD-dependent glyceraldehyde-3-phos- officially recognized in 1984 (25). phate dehydrogenase, indophenol oxidase, and phosphoglu- In the last few years, multilocus enzyme electrophoresis comutase were run in buffer system F (Tris maleate, pH 8.2). (MEE) has been used successfully with bacteria to analyze Specific staining for catalase was performed as described by various epidemiologic and taxonomic problems (17,27). This Harris and Hopkinson (8). The statistical analysis of the data method allows not only differentiation of strains, but also was done with a computer program designed by T. S. estimation of the genomic relatedness of strains, and their Whittam and R. K. Selander as described elsewhere (27). affiliation with species or subspecies. We recently found that DNA-DNA hybridization. DNA-DNA hybridization was a strain identified as L. ivanovii by using conventional performed at 60°C by using the S1 nuclease-trichloroacetic biochemical markers clearly belonged to a genomic group acid method described by Grimont et al. (7) and Rocourt et that has not been described previously when it was exam- al. (21). Bacteria were lysed as described below. Cells were ined by MEE. In this study, we analyzed more L. ivanovii grown for 48 h at 37°C in six Roux flasks containing 150 ml strains by using MEE and identified other members of this of Columbia agar, harvested, and washed in 20 ml of 0.1X group, which we characterized further by using their rRNA SSC (IxSSC is 0.15 M NaCl plus 0.015 M sodium citrate). gene restriction patterns and the results of DNA-DNA They were then incubated for 1 h at 37°C in 6 ml of a hybridization experiments. lysozyme solution (10 mM sodium phosphate-20% sucrose [pH 7.01 containing 0.2% lysozyme [Appligene, Illkirch, France]), lysed by adding 48 ml of a proteinase K solution * Corresponding author. (10 mM Tris-HC1 [pH 8.01, 1 mM EDTA, 1.25% sodium 69 70 BOERLIN ET AL. INT.J. SYST.BACTERIOL. TABLE 1. Analysis of L. ivanovii strains: with MEE, DNA-DNA hybridization, and rRNA gene restriction patterns 96 DNA Restriction Acid production with labeled DNA patterns from: from' : SDecies SerovaP Strain ET~ Origin' Strain N-acety l-P-D- SLCC Str~~~~lPEcoRI HindIII Ribose mannosamined 3769 L. ivanovii 5 CLIP 8457 1 (I) EIVl HIVl + France, sheep (abortion) L. ivanovii 5 CLIP 12547 1 (I) + France, sheep (abortion) L. ivanovii 5 CLIP 8459 1 (I) t France, sheep (abortion) L. ivanovii 5 CLIP 9441 1 (I) + Germany L. ivanovii 5 CLIP 2300 2 (I) EIVl HIVl + Belgium, human L. ivanovii 5 SLCC 2098 3 (1) 100 (0.3) 61 (3.6) EIV2 HIVl + Australia, sheep (liver) L. ivanovii 5 CLIP 12590 4 (I) + France, cheese L. ivanovii 5 SLCC 3769 4 (I) 100 (0.0) 70 (5.0) EIVl HIVl + Germany, environment L. ivanovii 5 CLIP 8181 5 (I) EIVl HIVl + Italy L. ivanovii 5 SLCC 4723 6 (I) EIVl HIV1 + Germany, bovine (nose) L. ivanovii 5 SLCC 4728 6 (I) + Germany, bovine (nose) L. ivanovii 5 SLCC 4729 7 (I) 103 (1.1) 65 (4.8) EIVl HIV2 + Germany L. ivanovii 5 CLIP 257 8 (I) + France, human (feces) L. ivanovii 5 CLIP 12510T 9 (I) 98 (0.6) 66 (5.6) EIVl HIVl + SLCC 2739T, ATCC 19119T L. ivanovii 5 SLCC 3887 10 (I) 106 (1.5) 68 (5.9) EIV 1 HIVl + Germany, environment L. ivanovii 5 SLCC 4054 11 (I) 99 (0.6) 81 (6.2) EIVl HIVl + Germany, cow (feces) L. ivanovii 5 SLCC 4306 12 (I) +_ Bulgaria L. ivanovii 5 SLCC 3765 13 (11) 60 (4.6) 107 (0.0) EN3 HIVl - Germany, corn leaves L. ivanovii 5 CLIP 2737 14 (11) 58 (6.4) 91 (0.6) HIVl - Czechoslovakia L. ivanovii 5 CLIP 12065 15 (11) 58 (5.3) 94 (0.2) EIV3 HIVl - Belgium, goat L. ivanovii 5 CLIP 1347 16 (11) 64 (4.9) 106 (0.0) EIV3 HIVl - France, dormouse L. ivanovii 5 CLIP 12229 17 (11) 62 (3.1) 100 (0.0) - France, food L. ivanovii 5 CLIP 6645 18 (11) 64 (4.7) 107 (0.6) EIV4 HIV3 - Switzerland L. monocytogenes 1/2 CLIP 14531T 16 ATCC 15313T L. monocytogenes 1l2a CLIP 12498 16 ATCC 35152 L. monocytogenes 4b CLIP 12505 16 ATCC 19115 L. innocua 6a CLIP 12511T 16 ATCC 33O9OT L. innocua 6b CLIP 12512 18 ATCC 33091 L. seeligeri 1/2b CLIP 12513T 42 (7.3) ATCC 35967T L. seeligeri us SLCC 3990 37 L. welshimeri 6b CLIP 12514T 17 ATCC 35897T L. welshimeri 6a SLCC 5332 19 L. grayi NA CLIP 125MT 4 ATCC 19120T L. grayi NA CLIP 640 3 L. murrayi NA CLIP 125MT 8 ATCC 25401T L. murrayi NA CLIP 12516 15 ATCC 25402 US, undesignated serovar; NA, not applicable. The ETs are listed in the same order as in Fig. 1; cluster designations are indicated in parentheses. ' Percentage of relative binding at 60°C. The values in parentheses are AT,,, values (in degrees Celsius). After 18 to 24 h. ' ATCC, American Type Culture Collection, Rockville, Md. dodecyl sulfate, 20 mg of proteinase K [Appligene]), and solution was filtered to sterility. The methyl red test was incubated overnight at 37°C. The DNA was finally purified performed in MR-VP medium (Difco). by sequential phenol-chloroform extractions. DNAs from strains SLCC 3769 and CLIP 12229T (T = type strain) were RESULTS radioactively labeled by nick translation. rRNA gene restriction patterns. rRNA gene restriction The 23 L. ivanovii strains which we studied by using MEE patterns were determined as described by Jacquet et al. (12) were assigned to 18 electrophoretic types (ETs) (Table 1and by using cloned rDNA (genes coding for rRNA) from Bacil- Fig.
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