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Roseiflexus Castenholzii Gen. Nov., Sp. Nov., a Thermophilic, Filamentous

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Roseiflexus Castenholzii Gen. Nov., Sp. Nov., a Thermophilic, Filamentous International Journal of Systematic and Evolutionary Microbiology (2002), 52, 187–193 Printed in Great Britain Roseiflexus castenholzii gen. nov., sp. nov., a thermophilic, filamentous, photosynthetic bacterium that lacks chlorosomes 1 Research Institute of Satoshi Hanada,1 Shinichi Takaichi,2 Katsumi Matsuura3 Biological Resources, 1 National Institute of and Kazunori Nakamura Advanced Industrial Science and Technology (AIST), Tsukuba Central 6, Author for correspondence: Satoshi Hanada. Tel: j81 298 61 6590. Fax: j81 298 61 6587. 1-1-1 Higashi, Tsukuba e-mail: s-hanada!aist.go.jp 305-8566, Japan 2 Biological Laboratory, T Nippon Medical School, A novel thermophilic, photosynthetic bacterium, designated strain HLO8 , was Kawasaki 211-0063, Japan isolated from a bacterial mat in a Japanese hot spring. Morphologically, the 3 Department of Biology, isolate was an unbranched multicellular filament with a cell diameter of Tokyo Metropolitan 08–10 µm. The bacterium was red to reddish-brown in colour and formed a University, Hachioji distinct red bacterial mat in the natural environment. It was able to grow 192-0307, Japan photoheterotrophically under anaerobic light conditions and also chemoheterotrophically under aerobic dark conditions. Optimal growth occurred at 50 SC and pH 75–80. The cells contained bacteriochlorophyll (Bchl) a and γ-carotene derivatives as photosynthetic pigments, but lacked Bchl c and chlorosomes. Cellular fatty acids in the isolate were mainly C16:0, C14:0 and C15:0. The major quinone was menaquinone-11. The DNA GMC content was 620 mol% (by HPLC). Phylogenetic analysis based on 16S rDNA sequencing suggested that the isolate belonged to the anoxygenic filamentous phototrophic bacteria represented by Chloroflexus aurantiacus, but was clearly distant from all members in this group (the sequence similarities between the isolate and its relatives were less than 838%). Based on genotypic and phenotypic data, the name Roseiflexus castenholzii gen. nov., sp. nov. is proposed for this isolate; the type strain is HLO8T (l DSM 13941T l JCM 11240T). Keywords: Roseiflexus castenholzii, gen. nov., sp. nov., anoxygenic photosynthesis, thermophiles, bacterial mats, gliding motility INTRODUCTION a key organism in considering the origin of photo- synthesis and the evolutionary process of photo- The multicellular filamentous phototrophic bacterium synthetic systems. Another species, Chloroflexus Chloroflexus aurantiacus was first described by Pierson aggregans, has been described in this genus (Hanada et & Castenholz (1974). Since this bacterium differed al., 1995). from the classical photosynthetic bacteria in many Chloroflexus aurantiacus respects at the time, a new family of phototrophic The group represented by bacteria was created for it (the family Chloroflexaceae; was named the anoxygenic filamentous phototrophs (Pierson & Castenholz, 1995). This photosynthetic Tru$ per, 1976). Phylogenetic analysis based on 16S Oscillochloris rRNA gene sequence data revealed that the bacterium group includes some other genera: et al Chloronema is not closely related to any other photosynthetic (Keppen ., 1994, 2000), (Dubinina & Heliothrix et al bacterium and forms the deepest branch among Gorlenko, 1975) and (Pierson ., 1985). Chloroflexus phototrophic bacteria (Oyaizu et al., 1987). The genus In addition, several -like bacteria have et al Chloroflexus, therefore, has received much attention as been observed in marine environments (Pierson ., 1994). Filamentous morphology and gliding motility ................................................................................................................................................. are typical of these phototrophic bacteria, most of Abbreviations: Bchl, bacteriochlorophyll; MK, menaquinone; RCR, Rabbit which possess light-harvesting apparatus called Creek Red. chlorosomes, which are intracellular vesicles contain- The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene ing bacteriochlorophyll (Bchl) c or d. This notable sequence of strain HLO8T is AB041226. photosynthetic apparatus is regarded as a typical 01908 # 2002 IUMS 187 S. Hanada and others feature in the anoxygenic filamentous phototrophs. after a few weeks. Enrichment of pure cultures was es- tablished using the same medium (pH 7n5) in screw-cap An exception is Heliothrix oregonensis which has no −# chlorosomes. H. oregonensis is an interesting fila- bottles at 50 mC under incandescent light (30 W m )orin mentous phototroph in that it contains Bchl a as the flasks shaken vigorously (200 r.p.m.) in the dark at the same temperature. 02YE medium (pH 7 5) was also used to sole chlorophyll species, but has not been cultured n " culture the strain. This medium contained (l− ): 02% yeast axenically. This bacterium was described as a co- n extract (Difco), 0n38 g KH#PO%,0n39 g K#HPO%,0n5g culture with the non-phototrophic bacterium, Iso- (NH%)#SO%, 1 ml vitamin mixture and 5 ml basal salt sphaera pallida (Pierson et al., 1985). solution. The vitamin mixture and basal salt solution were For several years, distinct red-coloured bacterial mats the same as those used in PE medium (Hanada et al., 1995). consisting of filamentous phototrophic bacteria have Morphology. The size, shape and ultrastructure of the cells been found in several neutral to alkaline hot springs in were examined by phase-contrast microscopy and trans- Japan. These filaments contained Bchl a and some mission electron microscopy. For transmission electron c microscopy, a centrifuged cell pellet was fixed with 5% (v\v) carotenoids as photopigments, but no Bchl has been glutaraldehyde and 1% (v\v) osmium tetroxide. Ultrathin detected. Morphological and spectroscopic features sections of the sample embedded in epoxy resin (Kushida, resembled those of H. oregonensis. Similar bacterial 1980) were prepared with a Reichert ultra-microtome. mats have also been observed in hot springs in Samples were stained with uranyl acetate and lead citrate, Yellowstone National Park (Boomer et al., 2000; and examined using a Hitachi H-7000 transmission electron Pierson & Castenholz, 1995). However, filamentous microscope. Gliding motility was determined by micro- bacteria like H. oregonensis have not been success- scopically observing 1-week-old colonies on an agar plate fully isolated, despite of the endeavours of many (PE medium, pH 7n5), ensuring that the tips of filaments researchers. glided out. Nutritional and physiological tests. For nutritional tests, Recently, a distinct red-coloured bacterial mat de- 5 ml medium containing one of various compounds as the veloped in Nakabusa hot spring in Japan [M. Sugiura, sole carbon and energy source to a final concentration of M. Takano and K. Toda (all Nagoya University), S. 0n25% (w\v) was used in a multi-well plate (12 wells). The −" Kawakami (Gifu University) and S. Hanada]. It was medium (pH 7n5) basically contained (l ): 0n38 g KH#PO%, predominantly composed of a filamentous photo- 0n39 g K#HPO% as a buffer, 0n5 g (NH%)#SO% as a nitrogen trophic bacterium containing Bchl a. The filamentous source, 1 ml vitamin mixture and 5 ml basal salt solution (see bacterium was isolated from the bacterial mat. The above). The following 18 compounds were used for the test: isolate, designated strain HLO8T, was a chlorosome- aspartate, glutamate, glycine, acetate, butyrate, citrate, less, gliding, filamentous, phototrophic bacterium malate, pyruvate, succinate, glucose, mannose, ethanol, glycerol, lactate, methanol, mannitol, Casamino acids and resembling H. oregonensis. In this paper, the distinct T yeast extract. All organic carbon sources were neutralized properties of strain HLO8 are described and a new and sterilized before addition. Each plate was incubated at taxon is proposed for the isolate. 50 mC under the following three conditions: anaerobically in the light, anaerobically in the dark and aerobically METHODS in the dark. Anaerobic conditions were achieved with an AneroPack system (Mitsubishi Gas Chemical). Photoauto- Habitat and isolation. Strain HLO8T was isolated from a trophic growth was tested with NaHCO$ (50 mM) as a bacterial mat in Nakabusa hot spring (Nagano Pref., Japan). carbon source and Na#S : 9H#O(0n2or0n4 mM) or Na#S#O$ The bacterial mat was well developed on a concrete wall in (3 mM) as electron donor. The results (OD at 660 nm) were the outflow from the spring. The temperature and pH ranges recorded after 1 week incubation. For estimation of the of hot water in the site were 40–60 mC and pH 7n8–8n2, optimal temperature range for growth, the isolate was respectively. The bacterial mat mainly consisted of three aerobically cultured in PE medium (pH 7n5) at the following zonal layers predominantly formed by phototrophic bac- temperatures: 35, 40, 45, 50, 55, 60 and 65 mC. Growth at teria. Each of the layers had a distinctive coloration (dark various pH values was also determined at 50 mCinPE green, brown and red in colour). The surface of the mat was medium that was buffered by 10 mM potassium phosphate mainly occupied by dark green and brown coloured layers. buffer (pH 6, 7 and 8) or 10 mM sodium glycine buffer (pH The dark green layer was composed mainly of thermophilic 9 and 10). cyanobacteria and the brown layer was due to Chloroflexus Spectroscopy and pigment analyses. Cells were collected sp. In addition to these, there was a distinct red layer from 1-week-old cultures in 02YE medium and were washed underneath the dark green and brown layers. The red layer and disrupted by sonication (140 W, 3 min) in potassium was on the concrete wall
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