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Achromobacter Xylosoxidans (Yabuuchi and Yano) and Proposal of Achromobacter Ruhlandii (Packer and Vishniac) Comb

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Achromobacter Xylosoxidans (Yabuuchi and Yano) and Proposal of Achromobacter Ruhlandii (Packer and Vishniac) Comb Microbiol. Immunol., 42(6), 429-438, 1998 Emendation of Genus Achromobacter and Achromobacter xylosoxidans (Yabuuchi and Yano) and Proposal of Achromobacter ruhlandii (Packer and Vishniac) Comb. Nov., Achromobacter piechaudii (Kiredjian et al.) Comb. Nov., and Achromobacter xylosoxidans Subsp. denitrificans (Roger and Tan) Comb. Nov. Eiko Yabuuchi*,', Yoshiaki Kawamura2, Yoshimasa Kosako3, and Takayuki Ezaki2 'Departmentof Microbiologyand Immunology , AichiMedical University,Faculty of Medicine,Aichi 480-1195, Japan, 'Depart- ment of Microbiology, Gi;fu UniversityMedical School, Gifu, Gifu 500-8705, Japan, and'Institute of Physical and Chemical Research, RIKEN, Wako,Saitama 351-0198, Japan ReceivedMarch 9, 1998. AcceptedMarch 25, 1998 Abstract: Based on the results of GC content determination and 16S rRNA sequence analysis among the type strains of Achromobacter xylosoxidans, 4 Alcaligenes species, 5 Bordetella species, and 12 species of 4 other genera, the separation of genus Achromobacter Yabuuchi and Yano 1981, with the type species Achro- mobacter xylosoxidans, is confirmed. Alcaligenes ruhlandii (Packer and Vishniac) Aragno and Schlegel 1992 is a distinct species and not a senior synonym of Achromobacter xylosoxidans. Alcaligenes ruhlandii and Alcaligenes piechaudii Kiredjian et al 1986 are transferred to genus Achromobacter. Thus 2 new combi- nations, Achromobacter ruhlandii (Packer and Vishniac) and Achromobacter piechaudii (Kiredjian et al) are proposed; their type strains are ATCC 15749 and ATCC 43552, respectively. Alcaligenes denitrificans Riiger and Tan 1983 is also transferred to genus Achromobacter and ranked down to the subspecies of Achro- mobacter xylosoxidans. Thus a new subspecies name, Achromobacter xylosoxidans subsp. denitrificans (Riiger and Tan) is proposed. The type strain of the subspecies is ATCC 15173. This proposal automatically creates type subspecies, Achromobacter xylosoxidans subsp. xylosoxidans, with type strain ATCC 27061. An emended description of genus Achromobacter and of type species Achromobacter xylosoxidans are given. Key words: Achromobacter xylosoxidans, Achromobacter ruhlandii, Achromobacter piechaudii, Achro- mobacter xylosoxidans subsp. denitrificans The species name Achromobacter xylosoxidans was from human ear discharge. More than 70 characters of first proposed in 1971 (24) for the 7 strains isolated 55 strains of A. xylosoxidans, including type strain for the *Address correspondence to Dr. Eiko Yabuuchi, Omiya 4-19- Japan; GC, Guanine plus cytosine; GIFU, Department of Micro- 18, Asahi-ku, Osaka, Osaka 535-0002, Japan. E-mail: Achei- biology, Gifu University School of Medicine, Gifu, Japan; IAM, 08 @fa2.so-net.or. jp Institute of Applied Microbiology, University of Tokyo, Tokyo, Japan; JCM, Japan Collection of Microorganisms, RIKEN, Saita- Abbreviations: ATCC, American Type Culture Collection, ma, Japan; LMG, Laboratorium voor Microbiologie, Universiteit Maryland, USA; CCM, Czech Collection of Microorganisms, Gent, Gent, Belgium; NAD, nicotinamide adenine dinucleotide; Masaryk University, Brno, Tvrdeho, Czech Republic; CDC, Cen- ND, no datum; NCIB, National Collection of Industrial Bacteria, ters for Disease Control and Prevention, Georgia, USA; comb. Aberdeen, Scotland; NCTC, National Collection of Type Cul- nov., combinatio nova=new combination; Cu, copper; DSM, tures, London, England; NJ, neighbor-joining; OF, oxidation-fer- Deutsche Sammlung von Mikroorganismen and Zellkulturen, mentation; RH, Rudolph Hugh, Department of Microbiology, Braunschweig, Germany; EY, Eiko Yabuuchi, Department of George Washington University School of Medicine, Washing- Microbiology and Immunology, Aichi Medical University, Aichi, ton, D.C., USA; SSC, saline-sodium citrate; subsp., subspecies. 429 430 E. YABUUCHI ET AL species (ATCC 27061), were described in 1974 (25). ferred the species to genus Alcaligenes and proposed a Because the Judicial Commission has been asked by new combination Alcaligenes ruhlandii (Packer and Hendrie et al (10) to reject the genus name Achro- Vishniac) for the peritrichous hydrogen bacterium. They mobacter on the basis that no type strain of the type later described that an NAD-specific soluble hydroge- species Achromobacter liquefaciens exists, the com- nase, not accompanied by a membrane-bound hydro- mission agreed (11) at a meeting on 3 September 1978 to genase (2), was encountered in both A. ruhlandii and A. omit the name from the Approved Lists of Bacterial xylosoxidans. They referred to Alcaligenes ruhlandii and Names (20). Thus the genus name Achromobacter was Alcaligenes denitrificans as the synonyms of Alcali- not included in the Approved Lists and lost its standpoint genes xylosoxidans Kiredjian et al (vide p. 370). Kersters in nomenclature. However, the name was not included and De Ley (13) also treated A. ruhlandii as a synonym in the list of rejected generic names. In accordance of "Alcaligenes denitrificans subsp. xylosoxidans." If A. with Rule 28a and Provisional Rule B3 of the Bacterio- xylosoxidans and A. ruhlandii are synonymous, the spe- logical Code (1975 Revision) (7), Achromobacter cific epithet of the former species must be ruhlandii, xylosoxidans (ex Yabuuchi and Ohyama 1971) was which precedes over xylosoxidans. revived for the same organism to which the name was Based on phenotypic characteristics, DNA base com- originally applied, and the new name Achromobacter, not position, DNA-DNA similarity, and 16S rRNA sequence "Achromobacter ," Bergey et al 1923 was proposed in analysis, the emendation of Achromobacter as a separate which A. xylosoxidans was placed as the type species. genus and its type species Achromobacter xylosoxidans The strain ATCC 27061 was designated as the type are described, and three new combinations, Achro- strain of A. xylosoxidans (26). mobacter ruhlandii, Achromobacter piechaudii, and Alcaligenes denitrificans (Jensen) Monias 1928 was Achromobacter xylosoxidans subsp. denitrificans, are listed in the Index Bergeyana as a validly published proposed. legitimate name (3). Although strain NCTC 8582 was designated as the type for the species, Alcaligenes de- Materials and Methods nitrificans Leifson and Hugh 1954 (15) was illegitimate because the specific epithet denitrificans is the later Bacterial strains. Histories and corresponding num- homonym within the same genus (Rule 25d). Hendrie, bers of the 6 type strains for 6 species of 3 genera are list- Holding, and Shewan in 1974 (10) erroneously consid- ed in Table 1. The strains were inoculated on Bacto-heart ered A. denitrificans Leifson and Hugh as a subjective infusion (HI) agar and incubated at 37 C unless otherwise synonym of Alcaligenes faecalis Castellani and Chalmers stated. (5), and they requested the Judicial Commission to issue Base composition of DNA. DNA base composition of an Opinion to reject the name A. denitrificans. A. deni- Alcaligenes ruhlandii EY 391 8Twas determined by high trificans was excluded from the Approved Lists. On the performance liquid chromatography as described previ- basis of DNA base composition, DNA homology, and ously (9). The calculation of the mol% GC was based on nitrate reduction, Ruger and Tan revived the name the Escherichia coli K-12 strain DNA as a standard Alcaligenes denitrificans in 1983 as a separate new (51.1 mol% GC). species (18). DNA-DNA hybridization. DNA-DNA similarities In 1984, Kersters and De Ley transferred Achro- among the type strains of Achromobacter xylosoxidans, mobacter xylosoxidans to genus Alcaligenes and pro- Alcaligenes denitrificans, Alcaligenes ruhlandii, Alcali- posed two new subspecies, A. denitrificans subsp. deni- genes piechaudii, and Bordetella bronchiseptica were trificans and A. denitrificans subsp. xylosoxidans (13). determined by quantitative microplate DNA-DNA Because the epithet xylosoxidans has precedence over hybridization as described previously (8). DNAs from 6 denitrificans, the latter subspecific name was announced type strains were reassociated with biotin-labeled DNAs as illegitimate (16). In 1986, Kiredjian et al (14) cor- from the type strains of Achromobacter xylosoxidans rected these subspecies names as Alcaligenes xylosoxi- and Alcaligenes ruhlandii at 51 C (stringent condition) by dans subsp. xylosoxidans and Alcaligenes xylosoxidans using 2 X SSC and 50% formamide. subsp. denitrificans. The 16S rRNA gene sequences and their phylogenet- Ruhland (19) described hydrogen-oxidizing autotroph- ic analyses. The 16S rRNA gene sequences of the type ic bacteria and named them as Knallgasbakterien. In strains of Alcaligenes ruhlandii and Alcaligenes 1955, Packer and Vishniac (17) proposed the new name piechaudii from positions 45 to 1380 (E. coli numbering) Hydrogenomonas ruhlandii for a facultatively autotroph- were determined by the method described previously ic hydrogen-oxidizing (Knallgas) bacterium, without (12), and the results were deposited into the DNA Data designating type strain. Aragno and Schlegel (1) trans- Bank of Japan under accession numbers AB010840 and GENUS ACHROMOBACTER, EMENDATION 431 Table 1. Histories and corresponding number of 6 type strains of Achromobacter, Alcaligenes, and Bordetella species ATCC, American Type Culture Collection, Maryland, USA; DSM, Deutsche Sammlung von Mikroorganismen and Zellkulturen, Braun- schweig, Germany; EY, Eiko Yabuuchi, Department of Microbiology and Immunology, Aichi Medical University, Aichi, Japan; GIFU, Department of Microbiology, Gifu University School of Medicine, Gifu, Japan; IAM, Institute of Applied Microbiology,
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