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Transfer of Bacteroides Clostridiiformis Subsp. Clostridiiformis to the Genus INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Apr. 1976, p. 205-211 Vol. 26, No. 2 Copyright 0 1976 International Association of Microbiological Societies Printed in U.S.A. Transfer of Bacteroides clostridiiformis subsp. clostridiiformis (Burri and Ankersmit) Holdeman and Moore and Bacteroides clostridiiformis subsp. girans (Prevot) Holdeman and Moore to the Genus Clostridium as Clostridium clostridiiforme (Burri and Ankersmit) comb. nov.: Emendation of Description and Designation of Neotype Strain ELIZABETH P. CAT0 AND CAROLYN W. SALMON Anaerobe Laboratory, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061 Twenty-five strains of bacteria with characteristics that conform to those given in the original and subsequent descriptions of the organism currently known as Bacteroides clostridiiformis (Burri and Ankersmit) Holdeman and Moore have been found to produce heat-resistant spores, which are often difficult to detect. Motility, also difficult to demonstrate in these strains, was found to be a variable characteristic within strains. We propose that B . clostridiiformis subsp. clostridiiformis (Burri and Ankersmit) Holdeman and Moore and B . clostridiiformis subsp. girans (Prevot) Holdeman and Moore be transferred to Clostridium as Clostridium clostridiiforme (Burri and Ankersmit) comb. nov. Prevot’s strain 171 I (= ATCC 29084 = VPI 3303), placed by Prevot in Ristella clostridiiformis, is designated as the neotype strain. Previously undescribed characteristics of this species are presented. In 1906, Ankersmit (1) described an organism formis (sic) in all of the main characteristics isolated in the laboratory of R. Burri, Zurich, given in Ankersmit’s description except that from a bovine intestinal tract and named it cells were motile in young cultures. Bacterium clostridiiforme. It was described as Choukevitch stated that, after the cultures an obligately anaerobic, gram-negative rod, 2.0 were more than 24 h old, the organism lost its to 3.0 pm long by 0.75 pm wide, spindle shaped, motility because of the acid produced. He con- with sharply pointed ends. Cells were usually cluded that his isolate from the horse was a in pairs, although sometimes they occurred in variant of B. clostridiiforme Ankersmit. short chains. Although the cells morphologi- After the generic name Bacterium was re- cally resembled small clostridia, even with oc- jected by the International Committee on No- casional swellings, spores were not observed, menclature of Bacteria (9), strains conforming and the cells did not survive heating for 15 min to the original descriptions of B. clostridiiforme at 80 C. Surface colonies on glucose agar were have led a peripatetic taxonomic existence. The 1.0 to 1.5 mm in diameter, circular, entire, various names under which these strains have grayish, and somewhat translucent with a soft been described and studied have been well doc- consistency and a crystalline appearance. Colo- umented by Holdeman and Moore (6). Until nies in glucose agar deeps were lenticular and 1973, names that had been accepted as validly semiopaque with a smooth edge. After 2 days, published and legitimate (2) were Eggerthella there was stringy growth at least 1.0 cm below dostridiiformis (Burri and Ankersmit) Be- the surface, and some gas formation was evi- erens, Castel, and Fievez (H. Beerens, M. M. dent. With alkaline pyrogallol to achieve an- Castel, and L. Fievez, International Congress aerobiosis, there was no visible growth in gela- for Microbiology, Montreal, 1962, Abstr. 120) tin after 10 days and no digestion of milk. In for the nonmotile strains and FusociZZus girans glucose broth, there was heavy turbidity, much Prevot (14) and Fusobacterium girans (Prevot) gas, and strong acidity. It was assumed that Macdonald (J. B. Macdonald, Ph.D. thesis, volatile acids were not formed because the Univ. of Toronto, Toronto, Canada, 1953) for broth had no odor. No motility was detected. the motile strains. In 1973, the International In 1911, Choukevitch (3) reported the isola- Subcommittee on Taxonomy of the Anaerobic, tion, from the large intestine of a horse, of an Gram-Negative Rods recommended that all an- organism that closely resembled B . clostridie- aerobic, gram-negative, nonmotile or peritri- 205 206 CAT0 AND SALMON INT. J. SYST.BACTERIOL. chous, nonsporeforming rods that did not pro- all members of the same species of Clostridiurn, duce butyric acid from the fermentation of car- We have, therefore, reexamined 25 strains re- bohydrate be placed in the genus Bacteroides. ceived from the Pasteur Institute, Paris, se- Because these organisms produced formic, lected because they resembled morphologically acetic, and sometimes traces of lactic and suc- the organism originally described by Ankers- cinic acids, as well as ethanol (5),the nonmotile mit (1) and resembled biochemically and meta- strains were named Bacteroides clostridiifor- bolically those organisms on which later mis subsp. clostridiiformis (Burri and Ankers- emended descriptions of B . clostridiiforrnis mit) Holdeman and Moore and the motile var- were based (4, 6, 14-17). iants were named Bacteroides clostridiiformis subsp. girans (Prkvot) Holdeman and Moore MATERIALS AND METHODS (12). Bacterial strains. The 25 strains studied, their All of these classifications were based on the sources where known, and the names given to them assumption that the organisms were nonspor- are listed in Table 1. These strains were identified in ing, gram-negative rods. However, in 1967 the laboratory of A.-R. Prevot at the Pasteur Insti- tute, Paris. Sixteen of them were also studied exten- Reinhold et al. reported (18) that, in their indi- sively by M. Sebald (19) in the same Institute. vidual laboratories, a labeled strain of Egger- Strain 3303 was kindly provided by H. Beerens, thella clostridiiformis (syn.: Ristella clostridi- Pasteur Institute, Lille; the rest were supplied by iforrnis) (Prkvot 171 I, Beerens and Tahon 22) Dr. Prevot. Two strains (0315 and 0316) were origi- did form spores and was gram positive and nally isolated from calf rumen by M. P. Bryant. We motile in young (3- to 4-h-old) cultures. At this tested freeze-dried cultures sent by him as well as time, many strains with the general character- freeze-dried cultures of his isolates received from istics of B . clostridiiformis were being isolated Dr. Prevot. Test results from both pairs of freeze- in our laboratory from normal human fecal dried cultures were similar and have been com- flora (131, and many that had been isolated bined. Methods. The strains described in this report from clinical specimens were being submitted were characterized by methods and procedures de- to us for identification (11). These strains dif- scribed previously (7). Special attention was given fered principally in motility, Gram reaction, to spores, heat resistance, motility, and flagella. and spore formation. It became important to Gram stains were made of young (2- to 3-h-old) determine whether these were not, in reality, cultures in media without carbohydrates to deter- '1AHI.E 1, Rlicteriill strains examined VPI Pasteur Institute (Paris) no. Previous identifications '1% c; + c no. (source) Pre'voF Sebaldb VPI 3303 171 I Ristrlla L.lo,stritiiiJbv~iis" Clostridiu rn s p . 48'1 5 3' 0292 2071 (plcurdl fluid) H istellLi hiacut a Cloytridium sp. 49 0293 2760A (throat) Kistella hiircuta Clostrid iu in s p . 0294 2894 Ki.sti~ll~rbiacuta Clostuidium sp. 0304 14lD Sphatwph o rus p dymorp h us Pusiformis po(ymorphus Bucteroides sp. 47 47 0315 B58 (calf rumen) K istplla birr cu ta Pusiformis bizcutus B. clostridiifbrmis subsp. clostridiiformis 55 0316 '190 (calf rumen) Kistclla hiacuta Pusitbr mis bill cu t us 13. cl ostrid iifo r m is suhsp. clostridiiforrnis 48 53 0432 85 II Kisti~llaclostridiiformis f'usif'ormis bidcutus Bacteroides sp. 0561 2198 Zuberc,Ila clostridiifbrmis Pusocillus girans Bucteroides biLrcutzrs 5 0 0562 2 150 (blocid) Zubrwlla clortridiiformis Fusocillus girans Clostridium spheno ides 46 4041 201 3 b'usvcillus girrrns Fusocillus girans Clostridium sphenoidcs 42 4042 215B I'uso cillus girir ns I'usocillus girans Clostridium sp. 5 0 404 3 161 1 H (abscess, appendicitis) Fuso cil1u.s gira ns Pusif'ormzs biacutus Clostridium sp, 46 4052 3484 (gangrenous appendix) I.'usocillus girans Clostridium sp. 4068 132 II K istella clostridiiformis l.'usocillics biacutus Bacteroides biacutus 48 40-41 4069 3219 (cervical cancer) KisttjlIa clostridiiformis Bacteroides biacutus 41 39 Potvin Zuberellil clostvidiitbrmis Clostridium sp. 4348 63-0 I,usocillus puns I'usocillus girans B. clostridiiformis subsp . clost ridiif o r m is 46 4349 627 (throat culture) f.'usocillus girlin5 I'usocillus girans Clostridium sp. 46 4867 3578B (Iivcr abscets) Ristella biacuta Bucteroider sp. 4870 4309 (abdominal absccss) Kistrlla biacuta Clostridium sp. 4971 2972 Kistellil biacuta Clostridium sp 5097 118-111 Ristelln biacuta I'usif iirmis b iu cu t us Clostridium sp 51-52 5115 320hR I:usiformzs nucleatus B. clostridiifnrmis subsp. clostridrifbrmis 5121 201-111 f(istella hiacutu buszformis biucutus Clostridium sp. 47 .'Prebt (18); 13Sebnld (21 ); "I.ater identified as Clostridium micuocporum by Reinhold et a1 (20); "Determined by Johnson by thermal melting point (Tm); 'Determined by Sebald by chromatographic analjpsis (21 ), VOL. 26, 1976 TRANSFER OF B. CLOSTRIDIIFORMIS 207 mine whether gram-positive cells were present. Cul- tures on chopped-meat slants incubated for 2 weeks at 30 C, as well as cultures showing swellings in Gram stains from any broth or plate, were inocu- lated into PY broth (7) with 0.5% starch and 1.0% glucose added. This inoculated broth was then heated for 10 min at 80 C and incubated at 37 C to detect heat-resistant cells. Tests for motility were made from 2- to 3-h-old chopped-meat broth cultures FIG. 1. Light micrograph of C. clostridiiforme and from the water of syneresis in peptone-yeast ATCC 29084 (24-h-old culture in peptone-yeast ex- extract-glucose agar slants. Flagella stains were tract broth). Bar = 10 pm. prepared as described previously (7). Production of H,S was determined in prereduced SIM medium (BBL).
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  • Genomic Background and Phylogeny of Cfia-Positive Bacteroides Fragilis
    antibiotics Article Genomic Background and Phylogeny of cfiA-Positive Bacteroides fragilis Strains Resistant to Meropenem-EDTA Sylvia Valdezate 1,* , Fernando Cobo 2 , Sara Monzón 2, María J. Medina-Pascual 1, Ángel Zaballos 3,4, Isabel Cuesta 2, Silvia Pino-Rosa 1 and Pilar Villalón 1 1 National Centre of Microbiology, Reference and Research Laboratory for Taxonomy, Instituto de Salud Carlos III, Majadahonda, 280220 Madrid, Spain; [email protected] (M.J.M.-P.); [email protected] (S.P.-R.); [email protected] (P.V.) 2 Department of Microbiology, Instituto Biosanitario de Granada, University Hospital of Virgen de las Nieves, Avda. Fuerzas Armadas s/n, 18014 Granada, Spain; [email protected] (F.C.); [email protected] (S.M.); [email protected] (I.C.) 3 Bionformatics Unit, Applied Services, Training and Research, Instituto de Salud Carlos III, Majadahonda, 280220 Madrid, Spain; [email protected] 4 Genomics Unit, Applied Services, Training and Research, Instituto de Salud Carlos III, Majadahonda, 280220 Madrid, Spain * Correspondence: [email protected]; Tel.: +34-91-822-3734; Fax: +34-91-509-7966 Abstract: Background: Bacteroides fragilis shows high antimicrobial resistance (AMR) rates and possesses numerous AMR mechanisms. Its carbapenem-resistant strains (metallo-β-lactamase cfiA- positive) appear as an emergent, evolving clade. Methods: This work examines the genomes, taxonomy, and phylogenetic relationships with respect to other B. fragilis genomes of two B. fragilis strains (CNM20180471 and CNM20200206) resistant to meropenem+EDTA and other antimicrobial Citation: Valdezate, S.; Cobo, F.; agents. Results: Both strains possessed cfiA genes (cfiA14b and the new cfiA28), along with other AMR Monzón, S.; Medina-Pascual, M.J.; mechanisms.
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