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Roseateles Depolymerans Gen. Nov., Sp. Nov., a New Bacteriochlorophyll A-Containing Obligate Aerobe Belonging to the P=Subclassof the Pro Teobacteria

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Roseateles Depolymerans Gen. Nov., Sp. Nov., a New Bacteriochlorophyll A-Containing Obligate Aerobe Belonging to the P=Subclassof the Pro Teobacteria International Journal of Systematic Bacteriology (1 999), 49,449-457 Printed in Great Britain Roseateles depolymerans gen. nov., sp. nov., a new bacteriochlorophyll a-containing obligate aerobe belonging to the P=subclassof the Pro teobacteria Tetsushi Suyama,’ Toru Shigematsu,’ Shinichi Takaichit2 Yoshinobu Nodasakaf3Seizo F~jikawa,~Hiroyuki Hosoya,’ Yutaka Tokiwa,’ Takahiro Kanagawa’ and Satoshi Hanadal Author for correspondence : Tetsushi Suyama. Tel : + 8 1 298 54 659 1. Fax : + 8 1 298 54 6587. e-mail: [email protected] ~~ 1 National Institute of Strains 61AT(T = type strain) and 6IB2, the first bacteriochlorophyll (BChI) a- Bioscience and Human containing obligate aerobes to be classified in the /?-subclassof the Technology, 1-1 Higashi, Tsukuba, lbaraki Profeobacteria, were isolated from river water. The strains were originally 305-8566,Japan isolated as degraders of poly(hexamethy1ene carbonate) (PHC). The organisms * Biological Laboratory, can utilize PHC and some other biodegradable plastics. The strains grow only Nippon Medical School, under aerobic conditions. Good production of BChl a and carotenoid pigments Kawasaki 21 1-0063,Japan is achieved on PHC agar plates and an equivalent production is observed under 3.4 School of Dentistry3 and oligotrophic conditions on agar medium. Spectrometric results suggest that Institute of Low BChl a is present in light-harvesting complex I and the photochemical reaction Temperature Science4, Hokkaido University, centre. The main carotenoids are spirilloxanthin and its precursors. Analysis of Sapporo 060, Japan the 165 rRNA gene sequence indicated that the phylogenetic positions of the two strains are similar to each other and that their closest relatives are the genera Rubriwiwax, ldeonella and Leptothrix with similarities of 96.3, 962 and 96-1%, respectively. The cells are motile, straight rods and contain poly-p- hydroxybutyrate granules. Ubiquinone-8 is the predominant quinone. Vitamins are not required for growth. The G+C content of genomic DNA is 66246.3 mol YO.Genetic and phenotypic features suggest that the strains represent a new genus in the p-subclass which is evenly distant from known genera. Consequently, the name Roseateles depolymerans gen. nov., sp. nov. is proposed for the strains; the type strain of Roseateles depolymerans is strain 61AT(= DSM 118133. Keywords : aerobic photosynthetic bacteria, bacteriochlorophyll a, /3-subclass, Proteobacteria, Roseateles depolymerans gen. nov., sp. nov. INTRODUCTION to as aerobic photosynthetic bacteria (Harashima et al., 1982; Shiba, 1989; Shimada, 1995). Although There are some species of bacteriochlorophyll (BChl) the function of their photosynthetic apparatus has not a-containing bacteria that cannot grow photosyn- yet been clarified, light-stimulated growth (Harashima thetically under anaerobic conditions even in light of et al., 1987; Yurkov & Gemerden, 1993) and photo- the effective wavelength. These organisms are referred synthetic activity (Harashima et al., 1982 ; Kortluke et al., 1997; Okamura et al., 1986; Shiba, 1984; Takamiya & Okamura, 1984) have been reported in Abbreviations: BChl, bacteriochlorophyll; FD-MS, field desorption mass some species of aerobic photosynthetic bacteria. spectrometry; LH-I, light-harvesting complex I; PHB, poly-0-hydroxybuty- rate; PHC, poly(hexamethy1ene carbonate); UQ-8, ubiquinone with 8 Yurkov & Gemerden (1993) hypothesized an advan- isoprene units. tage of having both photosynthetic and heterotrophic The GenBanUEMBLaccession numbers for the 165 rRNA gene sequences of metabolisms in terms of adaptation to the environment strains 61AT and 61B2 are AB003623 and AB003625, respectively. with altering light/dark conditions under aerobic 00785 0 1999 IUMS 449 T. Suyama and others conditions. Some physiological changes related to emulsified poly(hexamethy1ene carbonate) (PHC) as a sub- adaptation to light/dark have been reported (Takaichi strate at 30 "C (Suyama et al., 1998). et al., 1991;Tilden et al., 1997). The type strain of Rubrivivax gelatinosus (DSM 1709T= ATCC 1701lT = NCIB 8290T= LMG 43 1 1') used in this .Aerobic photosynthetic bacteria have been isolated study as a reference species was purchased from Deutsche from various environments : freshwater (Fuerst et al., Sammlung von Mikroorganismen und Zellkulturen (DSMZ, 1993), marine cyanobacterial mat (Yurkov et al., Braunschweig, Germany). 1994), cyanobacterial mat from warm/hot spring et al., 1997; & 1993; Culture media. The following media were used in the present (Hanada Yurkov Gemerden, study. The agar plates were prepared by adding 1-5% (w/v) Yurkov & Gorlenko, 1992, 1993; Yurkov et al., 1993) Bacto agar (Difco) to the media. PHC medium was used for and surfaces of seaweeds (Shiba, 1991; Shiba & isolation and maintenance of original culture line. CAV Simidu, 1982). Currently, aerobic photosynthetic bac- medium was used for the other physiological tests. teria are classified into the following genera : Erythro- bacter and Roseobacter for marine species; and Por- The PHC medium contained (13 1 g PHC (emulsified, number-average molecular mass Mn = 2000; Toagosei) ; 1 g phyrobacter, Erythromicrobium and Roseococcus for (NH,),SO,; 0.1 g yeast extract (Difco) ; 20 mg CaC1,. 2H,O; freshwater species. Recently, two genera, Sandara- 10 mg NaCl; 10 mg FeSO, . 7H,O ;0.5 mg Na,MoO, . 2H,O; cinobacter and Erythromonas, were separated from 0.5 mg Na,WO,. 2H,O; 0.5 mg MnSO, ; 60 mg surfactant Erythromicrobium (Yurkov et al., 1997). Furthermore, (Plysurf A210G; Daiichi Kogyo Seiyaku); 0.2 g KH,PO,; similar isolates have been reported from soil (Saitoh & and 1.6 g K,HPO, (pH 7-0). Nishimura, 1996), surfaces of plants (Urakami et al., The CAV medium contained (1-l): 2 g Casamino acids 1993), nodules of legumes (Evans et al., 1990), food, (Difco); 0.5 g (NH,),SO,; 1 ml vitamin mixture; 10 ml basal animal feed and sewage sludge (Nishimura et al., salt solution; and 25 ml 200 mM potassium phosphate 1981), some of which are currently classified into buffer (pH 7.0). The composition of the basal salt solution genera which have been considered as typical non- and the vitamin mixture were previously described (Hanada phototrophs: Acidiphilium (possessing zinc-substi- et al., 1997). tuted BChl a> (Wakao et al., 1996), Bradyrhizobium Physiological tests and determination of growth conditions. (Evans et al., 1990; Young et al., 1991) and Methylo- The ability of the strains to grow photosynthetically under bacterium (Green & Bousfield, 1983; Urakami et al., anaerobic conditions was investigated both on the agar 1993). So far, all of the genera described above have plates and in liquid culture in the light. The anaerobic or been phylogenetically classified into the a-subclass of semi-aerobic growth on agar plates was assessed in an the Proteobacteria. Five genera, Erythrobacter, Ery- anaerobic jar with Anaero Pack or Campylo Pack (Mitsu- thromicr o bium, Ery t hr om onas, Porphyr obac ter and bishi Gas Chemical), respectively. The photoheterotrophic Sandaracinobacter, a-4 growth was ascertained using PE medium (Hanada et al., belong to the group where 1995b), which contains acetate, glutamate and succinate as aerobic photosynthetic species are predominant and electron donors. The photoautotrophic growth in the pres- the others belong to the a-1 to a-3 groups, which ence of reduced sulfur compounds was determined in a contain close relatives of typical anoxygenic photo- medium containing (1-I): 0.5 g (NH,),SO,; 0.5 g Na, synthetic bacteria (Hanada et al., 1997; Shimada, S,O, .5H,O ;0.1 g Na,S .9H,O ;4.2 g NaHCO, ; 1 ml vitamin 1995;Turova et al., 1995;Young et al., 1991 ; Yurkov mixture; 5 ml basal salt solution (Hanada et al., 1997); and et al., 1994, 1997). No aerobic photosynthetic bac- a final concentration of 10 mM potassium phosphate buffer terium has been reported outside of the a-Proteo- (pH 7.0). bacteria. The growth rates as a function of temperature were a, determined in CAV medium. The vitamin requirement was Two new obligate aerobes containing BChl strain "C (= determined at 30 with special CAV medium lacking the 61AT DSM 11813T; T=type strain) and strain vitamin mixture and containing vitamin-free Casamino acids 61B2 (= DSM 1 1814), were isolated from river water (Difco). The final reading was obtained after nine serial by screening aliphatic polycarbonate-degrading micro- transfers. The growth rates at various pH were also organisms (Suyama et al., 1998). Phylogenetic analysis determined at 30 "C in a series of CAV media that were based on 16s rRNA comparisoiis revealed that these buffered by 10 mM sodium citrate (pH 3-6), 10 mM pot- strains belong to the p-subclass of the Proteobacteria; assium phosphate (pH 7-8) or 10 mM sodium/glycine buffer the strains are thought to be the first aerobic photo- (PH 9-1 1). synthetic bacteria found in this taxon. For the analysis of photosynthetic pigments, colonies In the present study, morphological, physiological, formed on PHC agar plate medium incubated for 3 d were used. Pigments were extracted from cells with acetone/ biochemical and genetic characteristics of the strains methanol (7 : 2, v/v). The crude extract was analysed with an are described and a new genus name, Roseateles HPLC system equipped with ap Bondapak C18 column depolymerans gen. nov., sp. nov., is proposed for the (8 x 100 mm; Waters) eluting with methanol (Takaichi & isolates. Shimada, 1992). Major carotenoids were purified from silica gel TLC (Merck) developed with n-hexane and acetone (4 : 1, METHODS v/v). Absorption spectra were recorded with a photodiode array detector (200-800 nm, MCPD-3600; Otsuka Elec- Origin of strains. Strains 61ATand 61B2 were isolated from tronics) attached to the HPLC apparatus (Takaichi & the Hanamuro River in Tsukuba, Ibaraki Prefecture of Shimada, 1992). The molar absorption coefficients in meth- Japan. The strains were isolated with a medium containing anol (90.6 rnM-'cm-' at absorption maxima for carotenoids 450 International Journal of Systematic Bacteriology 49 Roseateles depolyrnerans gen. nov., sp. nov. and 54.9 mM-lcm-l at 770 nm for BChl a) were used for RESULTS quantification.
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