Proposal of Sphingomonadaceae Fam. Nov., Consisting of Sphingomonas Yabuuchi Et Al. 1990, Erythrobacter Shiba and Shimidu 1982, Erythromicrobium Yurkov Et Al
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Microbiol. Immunol., 44(7), 563-575, 2000 Proposal of Sphingomonadaceae Fam. Nov., Consisting of Sphingomonas Yabuuchi et al. 1990, Erythrobacter Shiba and Shimidu 1982, Erythromicrobium Yurkov et al. 1994, Porphyrobacter Fuerst et al. 1993, Zymomonas Kluyver and van Niel 1936, and Sandaracinobacter Yurkov et al. 1997, with the Type Genus Sphingomonas Yabuuchi et al. 1990 Yoshimasa Kosako*°', Eiko Yabuuchi2, Takashi Naka3,4, Nagatoshi Fujiwara3, and Kazuo Kobayashi3 'JapanCollection of Microorganis ms,RIKEN (Institute of Physical and ChemicalResearch), Wako, Saitama 351-0198, Japan, 2Departmentof Microbiologyand Immunology , AichiMedical University, Aichi 480-1101, Japan, 'Departmentof Host Defense,Osaka City University, Graduate School of Medicine,Osaka, Osaka 545-8585, Japan, and Instituteof SkinSciences, ClubCosmetics Co., Ltd., Osaka,Osaka 550-0005, Japan ReceivedJanuary 25, 2000; in revisedform, April 11, 2000. Accepted April 14, 2000 Abstract:Based on the results of phylogeneticanalysis of the 16SrDNA sequences and the presence of N- 2'-hydroxymyristoyldihydrosphingosine 1-glucuronic acid (SGL-1)and 2-hydroxymyristicacid (non- hydroxymyristicacid in Zymomonas)in cellular lipids,a new family,Sphingomonadaceae, for Group 4 of the alpha-subclassof the classProteobacteria is hereinproposed and a descriptionof the familyis given.The familyconsists of six genera, Sphingomonas,Erythrobacter, Erythromicrobium, Porphyrobacter, Sandara- cinobacterand Zymomonas.Thus, all the validlypublished and currently known genera in Group 4 of the alpha-subclassof Proteobacteriabelong to Sphingomonadaceaefam. nov.Among them, type strains of two species, Porphyrobacter and Erythrobacter, Sandaracinobactersibiricus and Sphingomonasursincola, respectively,are facultativelyphotosynthetic due to bacteriochlorophyll(Bchl)-a. The type strains of two subspeciesof Zymomonasmobilis are facultativeanaerobes. The presenceof SGL-1together with the results of a phylogeneticanalysis of the 16SrDNA sequences recommends a newcriteria by whichto definethe new family Sphingomonadaceae.The type genus is SphingomonasYabuuchi et al. 1990. Keywords: Sphingomonadaceae fam. nov., New family,Proteobacteria, Alpha-subclass, Sphingoglycolipid *Address correspondence to Dr. Yoshimasa Kosako, Japan ismen and Zellkulturen, Braunschweig GmbH, Germany; EY, Collection of Microorganisms, RIKEN (The Institute of Physical Eiko Yabuuchi, Department of Microbiology and Immunology, and Chemical Research), Wako, Saitama 351-0198, Japan. Aichi Medical University, Aichi, Japan; GC, guanine plus cyto- Fax: x--81-48-462-4618. E-mail: [email protected] sine; GIFU, Department of Microbiology,Gifu University School of Medicine,Gifu, Japan; IAM, Institute of Applied Microbiology, University of Tokyo, Tokyo, Japan; IFO, Institute for Fermenta- Abbreviations: ACM, Australian Collection of Microorgan- tion Osaka, Osaka, Japan; JCM, Japan Collection of Microor- isms, Department of Microbiology, University of Queensland, ganisms, RIKEN (The Institute of Physical and Chemical Queensland, Australia; AMPC, amoxicillin; ATCC, American Research), Saitama, Japan; LMG, Laboratorium voor Microbi- Type Culture Collection, Mananas, Virginia, U.S.A.; comb. nov., ologie, Universuteit Gent, Gent, Belgium; PYA, peptone (1%)- combinatio nova= new combination; CVC, clavulanic acid; yeast extract (1%)-NaCI (0.5%) agar; RDP, Ribosomal Data- DDBJ, DNA Data Bank of Japan, Institute of Genetics, Mishima, base Project, Center for Microbial Ecology, Michigan State Uni- Shizuoka, Japan; DSM, Deutsche Sammlung von Mikroorgan- versity, Michigan, U.S.A.; SGL, Sphingoglycolipid, 563 564 Y. KOSAKO ET AL ATCC 10829, a type strain of Flavobacterium devo- the genus Sphingomonas. In addition to these, "Sphin- rans (Zimmermann 1890) Bergey et al. 1923"L, was a gomonas wittchii" was proposed by Yabuuchi et al for the high GC organism and found to have N-2'-hydrox- strain known as dibenzo-p-dioxin metabolizing strain ymyristoyl dihydrosphingosine 1-glucuronic acid (SGL- RW1 (personal communications). 1) in cellular lipids (35). From these and other fea- The class Proteobacteria Stackebrandt et al. 1988 tures, ATCC 10829 was reidentified as an strain of (24) was proposed for the phylogenetic taxon that Pseudomonas paucimobilis Holmes et al. 1977"L (9), includes the "purple bacteria and their relatives" which is listed in the approved list of bacterial names described by Woese et al (32). (22). Because strain ATCC 10829 was not a original On the basis of the results of the 16S rDNA sequence Zimmermann strain but a later misidentified organism, comparison, Takeuchi et al. reported in 1994 (27) that the the name F devorans could not be a senior synonym of genus Sphingomonas belongs to the alpha-subclass of the P paucimobilis. A similar component, SGL-1, was Proteobacteria and is a part of Group 4. Strains of fac- found in the cellular lipids of yellow-pigmented iso- ultatively photosynthetic species of four genera Por- lates originally identified as strains of Pseudomonas sp. phyrobacter, Erythrobacter, Sandaracinobacter and Eryth- including P paucimobilis, Flavobacterium sp. and Sphin- romicrobium, together with facultatively anaerobic gobacterium sp. In addition to this, the results of a Zyymomonasare also reported as belonging to Group 4 of phylogenetic analysis of partial nucleotide sequences the alpha-subclass of Proteobacteria. of the 16S rDNA led to the proposal of a new genus, In 1976, De Ley and Swing proposed an improved Sphingomonas Yabuuchi et al. 1990" with the type taxonomy and nomenclature of the genus Zymomonas species Sphingomonas paucimobilis (Holmes et al. 1977) Kluyver and van Niel 1936" (4). From the phenotypic Yabuuchi et al. 1990" (34). In this new genus, three new and genetic data, they unified "Z. anaerobica" subsp. species, S. adhaesiva, S. parapaucimobilis and S. "anaerobica" and "Z. anaerobica" subsp. "immobilis," yanoikuyae, and a new combination, S. capsulata (Leif- and raised Zymomonas mobilis (Lindner) De Ley and son 1962") Yabuuchi et al. 1990" were named and Swing 1976" to a species. The proposal of Z. mobilis described. Two other strains containing SGL-1 in their subsp. pomaceae" by De Ley and Swing automatically cellular lipids were differentiated from the above-men- created Z. mobilis subsp. mobilis. tioned species; the authors were reluctant to name them The genus Erythrobacter is made up of two species. because each of them was a single strain. Erythrobacter longus Shiba and Simidu 1982" (21) and Since then, 14 new species and three new combina- Erythrobacter litoralis Yurkov et al. 1994" (36) were tions of Sphingomonas have been validly named and proposed for an aerobic organism containing bacteri- described. The 14 new species are: S. macrogoltabidus ochlorophyll a. Takeuchi et al. 1993"; S. sanguis Takeuchi et al. 1993' Erythromicrobium ramosum Yurkov et al. 1994" was and S. terrae Takeuchi et al. 1993' (25); 3-ketolactose- proposed for a strain isolated from a marine cyanobac- producing S. rosa Takeuchi et al. 1995"; S. pruni terial mat (36). A new genus, Porphyrobacter Fuerst et Takeuchi et al. 1995v'; S. asaccharolytica Takeuchi et al. al. 1993", with a single type species, P. neustonensis 1995" and S. mali Takeuchi et al. 1995" (26); S. Fuerst et al. 1993", was proposed for aerobic bacteri- chlorophenolica Nohynek et al. 1995".(17); S. herbici- ochlorophyll-synthesizing bacteria (7). Another species, dovorans Zipper et al. 1996" (38); S. subarctica P. tepidarius, was proposed by Hanada et al. 1997 (8). Nohynek et al. 1996" (18); S. trueperi Kaempfer et al. The former was isolated from fresh water and budding 1997' (10); an aromatic-degrading species, S. aromati- multiplication was observed by electron microscopy. civorans Balkwill et al. 1997"'; S. subterranea Balk- The latter was a moderately thermophilic aerobe iso- will et al. 1997"'; and S. stygia Balkwill et al. 1997" (1). lated from a hot spring. Three species, Blastobacter natatoria Sly 1985' (23), The type strain of Sandaracinobacter sibiricus Yurkov "Rhizomonas" suberifaciens van Bruggen et al. 1990" et al. 1997".(37) was isolated from a freshwater algo- (30) and Erythromonas ursincola Yurkov et al. 1997' bacterial mat near hydrothermal sulfide-containing vents (37) were transferred to the genus Sphingomonas, and S. along a river bottom. natatoria, S. suberifaciens and S. ursincola were pro- In this study, with the two exceptions of unavailable posed (33). Publication of these three new combinations type strains of Sandaracinobacter sibiricus and the was listed in Validation List No. 70. After a phylogenetic unsuccessfully revived lyophile of S. herbicidovorans , we analysis, Pseudomonas echinoides Heumann 1962" was confirmed the distribution of sphingoglycolipid (SGL-1), transferred to the genus Sphingomonas as Sphingomonas morphological, physiological and biochemical charac- echinoides (Heumann 1962) Denner et al. 1999' (5). At teristics. The phylogeny of the 16S rDNA sequence present, 23 species are validly published as members of among the species in the alpha-4 group, including San- SPHINGOMONADACEAE KOSAKO AND YABUUCHI FAM. NOV. 565 daracinobacter sibiricus, was analyzed in order to elu- Phenotypic characterization and antimicrobial sus- cidate the possibility of proposing a new family to Group ceptibility tests. Morphologies of the cells of each strain 4 of the alpha-subclass of Proteobacteria. were observed by optical microscopy of Gram-stained preparations. Motility was observed by microscopy Materials and Methods