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Kluyvera: Buttiamella Ferragutiae Sp INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Jan. 1996, p. 50-63 Vol. 46, No. 1 0020-7713/96/$04.00+0 Copyright 0 1996, International Union of Microbiological Societies Emended Description of Buttiamella agrestis with Recognition of Six New Species of Buttiamella and Two New Species of Kluyvera: Buttiamella ferragutiae sp. nov., Buttiamella gaviniae sp. nov., Buttiamella brennerae sp. nov., Buttiamella izardii sp. nov., Buttiamella noackiae sp. nov., Buttiamella warmboldiae sp. nov., Kluyvera cochleae sp. nov., and Kluyvera georgiana sp. nov. HANS E. MULLER,'" DON J. BRENNER,2 G. RICHARD PATRICK A. D. GRIMONT,4 AND PETER UMPFER'? Staatliches Medizinaluntersuchungsamt, 0-38124 Braunschweig, and Fachgebiet Hygiene, Technische Universitat, D-13353 Berlin' Germany; Emerging Bacterial and Mycotic Diseases Branch, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia 303332; Division of Biochemistry, Walter Reed Army Institute uf Research, Washington, D. C. 20307-51003; and Unit6 des Enterobacthies, Institut National de la Santk et de la Recherche Mddicale Unit&389, Institut Pasteur, F-75724 Paris Cedex 15, France4 A total of 219 strains belonging to the genera Buttiuuxellu and Kluyveru were studied; 171 of these strains were isolated from mollusks, mainly snails and slugs, obtained from around the world. On the basis of DNA-DNA hybridization data, the strains were grouped into 11 genomospecies. A total of 44 phenotypic characters were used to differentiate the genera Buttiuuxellu and Kluyveru at the genus level and to identify genomospecies. There were significantly higher phenotypic probability distances between the genomospecies in the genus Butti- uuxella and the genomospecies in the genus Kluyveru than between the genomospecies in the same genus. There- fore, the existence of Buttiuuxellu and Kluyveru as different genera was confirmed. The existence of new species necessitated broadening the definitions of both genera. In two cases, two Buttiuuxellu species could not be quantitatively differentiated biochemically, and several other pairs of species could be separated only by the results of one biochemical test. Nonetheless, combinations of several characteristics were used to differentiate all of the species with levels of certainty ranging from log 10.79 to log 57.77 (calculated as probability dis- tances). The following new species are proposed Buttiuuxellaferragutiue (type strain, ATCC 51602 [DSM 9390]), Buttiuuxellu guviniue (type strain, ATCC 51604 [DSM 9393]), Buttiuuxella brennerue (type strain, ATCC 51605 [DSM 9396]), Buttiuuxella izardii (type strain, ATCC 51606 [DSM 9397]), Buttiuuxellu nouckiue (type strain, ATCC 51607 [DSM 9401]), Buttiuuxellu wumzboldiae (type strain, ATCC 51608 [DSM 9404]), Kluyveru cochleae (type strain, ATCC 51609 [DSM 9406]), and Kluyveru georgiunu (type strain, ATCC 51603 [DSM 94091). In 1976, a taxon designated group F was described by Gavini culture collection were more than 100 strains that were placed et al. (15). The strains belonging to group F were originally in a group designated enteric group 8. In 1981, Farmer et al. isolated from humans, soil, and water in the course of a study redefined the genus Kluyvera to include enteric group 8 along on the genus Citrobacter, and they were lactose positive, as are the named species Kluyvera ascorbata and Kluyvera cryocrescens members of the genus Citrobacter. However, these organisms and a third unnamed species (11). The genera Buttiauxella and differed from Citrobacter strains in several biochemical char- Kluyvera are generally similar phenotypically, although they acteristics, as well as in their DNA-DNA-hybridization char- can be differentiated. The members of these genera have dif- acteristics and guanine-plus-cytosine (G+ C) ratios (13, 14). ferent G+C contents and exhibit low levels of DNA related- Hence, the 17 strains were considered members of a new genus ness (14). in the family Enterobacteriaceae. This genus was named Butti- The frequent and profuse occurrence of Buttiauxella and auxella and contained a single species Buttiauxella agrestis. Kluyvera strains in snails and slugs is an intriguing finding. Four strains subsequently studied by Ferragut et al. were Numerous strains belonging to these previously rarely seen placed in the genus Buttiauxella but were not B. agrestis strains genera have been isolated. However, the phenotypic charac- (13). At the Centers for Disease Control and Prevention, three teristics that separate these genera did not allow clear assign- of these strains were placed in a group that was given the ment of these isolates at the genus level. The biochemical vernacular name enteric group 63, and the fourth was placed in reactions of the previously described species and the new iso- enteric group 64 (10). lates suggested that most of the new isolates belong to new Also in the Centers for Disease Control and Prevention species. In this paper we describe the results of a taxonomic study of Buttiauxella and Kluyvera strains. MATERIALS AND METHODS * Corresponding author. t Present address: Institut fur Angewandte Mikrobiologie, Justus- Bacterial strains. The Buttiauxella and Kluyveru strains used in this study are Liebig Universitat Giessen, D-35390 Giessen, Germany. listed in Table 1. The field strains were isolated from snails and slugs and samples 50 VOL. 46, 1996 NEW BUTTUUXELLA AND KLuM/ERA SPECIES 51 TABLE 1. Strains investigated in this study Serial Group Strain Labora- no. tory(ies)" Origin Other designation(s)b DNA group 1 (B. agrestis) 001' CDC 1176-81T (= CUETM 77-167T) 1, 4 Unpolluted soil, Franced ATCC 33320T 002 CUETM 77-157 4 Drinking water, France" 003 CUETM 78-3 4 Unpolluted soil, Franced 004 CUETM 78-5 4 Unpolluted soil, Franced 005 CUETM 78-8 4 Drinking water, Franced 006 CUETM 78-18 4 Unpolluted soil, Franced 007 CUETM 78-19 4 Drinking water, France" 008 CUETM 78-27 4 Drinking water, France" 009 CUETM 78-29 4 Drinking water, Franced ACTT 33994 010 CUETM 78-34 4 Unpolluted soil, France" ATCC 33995 01 1 CUETM 78-44 4 Drinking water, Franced 012' S3/3-162 3 Snail, Braunschweig, Germany DSM 9388 013" S3/3-203 3 Snail, Braunschweig, Germany 014 S3/4-204 3 Snail, Braunschweig, Germany 015 S3/4-556 3 Snail, Braunschweig, Germany 016 s3/4-775 3 Snail, Braunschweig, Germany 017' S3/4-776 3 Snail, Braunschweig, Germany 018' s3/4-779 3 Snail, Braunschweig, Germany 019 S314-871 3 Snail, Braunschweig, Germany 020 S3/4-1 098 3 Slug, Braunschweig, Germany 021' S3/5-201 3 Snail, Braunschweig, Germany 022' s315-757 3 Snail, Braunschweig, Germany 023" S316-333 3 Slug, Braunschweig, Germany DSM 9389 024" S3/7-896 3 Slug, Braunschweig, Germany 025' S3/7-897 3 Snail, Braunschweig, Germany 026' 5318-910 3 Slug, Salisbury, Great Britain 027 S3/9-488 3 Slug, Braunschweig, Germany 028 S3/9-602 3 Snail, Braunschweig, Germany 02Y S3/9-878 3 Snail, Braunschweig, Germany 03F S3/9-887 3 Slug, Braunschweig, Germany 031' S3110-769 3 Snail, Braunschweig, Germany 032' S3/11-533 3 Slug, Braunschweig, Germany 033' S3111-794 3 Snail, Braunschweig, Germany 034 S3/11-832 3 Snail, Braunschweig, Germany 035 S3111-859 3 Snail, Braunschweig, Germany 036 s3114-770 3 Snail, Braunschweig, Germany 037" s3114-1071 3 Slug, Braunschweig, Germany 038 S3/14- 1073 3 Slug, Braunschweig, Germany 039 S3/14-1080 3 Slug, Braunschweig, Germany 040 s3114-108 1 3 Slug, Braunschweig, Germany 04 1 S3/14-1082 3 Slug, Braunschweig, Germany 042' S3/14-1085 3 Slug, Braunschweig, Germany 043 s3114-1094 3 Slug, Braunschweig, Germany 044 S3/14-1096 3 Slug, Braunschweig, Germany 045 s3114-1099 3 Slug, Braunschweig, Germany 046 S3/14-1101 3 Slug, Braunschweig, Germany 047 S3114-1 127 3 Slug, Braunschweig, Germany 048 S3/14-1129 3 Slug, Braunschweig, Germany 049 s3114-1132 3 Slug, Braunschweig, Germany 050 S3/14-1146 3 Slug, Braunschweig, Germany 05 1 S3/14-1149 3 Slug, Braunschweig, Germany 052 S3/14-1166 3 Slug, Braunschweig, Germany 053' S3/13-692 3 Slug, Braunschweig, Germany DNA group 2 (enteric 05 4' CDC 1180-81T (= CUETM 78-31T) 1, 4 Unpolluted soil, France (13) ATCC 51602=, DSM 9390T group 63, B. ferragutiae) 055 CUETM 78-50 4 Drinking water, France (13) DSM 9391 056 CUETM 78-35 4 Unpolluted soil, France (13) 05 7 CUETM "H. alvei 125" 4 Unknown, France DNA group 3 (enteric 058' CDC 1175-81 (= CUETM 77-159) 1, 4 Unpolluted soil, France (13) DSM 9392 group 64, B. gaviniae) 059 Slll-895 3 Slug, Braunschweig, Germany 060 S1/1-978 3 Snail, Braunschweig, Germany 061 Slll-981 3 Snail, Braunschweig, Germany 062" Sl/l-984T 3 Snail, Braunschweig, Germany ATCC 51604, DSM 9393 063" S1/1-986 3 Snail, Braunschweig, Germany 064 s111-987 3 Snail, Braunschweig, Germany 065 s111-988 3 Snail, Braunschweig, Germany 066 s111-993 3 Snail, Braunschweig, Germany ~ Continued on following page 52 MULLER ET AL. INT. J. SYST.BACTERIOL. TABLE 1-Continued Labora- Serial Strain Origin Other designation(s)'' Group no. tory( ies)" 067 S1/1-996 3 Snail, Braunschweig, Germany 068 Sl/1-998 3 Snail, Braunschweig, Germany 069 S1/1-999 3 Snail, Braunschweig, Germany 070 s lil-1000 3 Snail, Braunschweig, Germany 071 S 1/1-1003 3 Snail, Braunschweig, Germany 072 S 1/1-1007 3 Snail, Braunschweig, Germany 073 Sl/l-1032 3 Snail, Braunschweig, Germany 074 Sl/l-1033 3 Snail, Braunschweig, Germany 075 Sl/l-1039 3 Snail, Braunschweig, Germany 076 Sl/l-1041 3 Snail, Braunschweig, Germany 077 Sl/l-1049 3 Snail, Braunschweig, Germany 078 Sl/l-1050 3 Snail, Braunschweig, Germany 079 Sl/l-105 1 3 Snail, Braunschweig, Germany 080 Sl/l-1116 3 Slug, Braunschweig,
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