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Bellilinea Caldifistulae Gen. Nov., Sp. Nov. and Longilinea Arvoryzae Gen. Nov., Sp. Nov., Strictly Anaerobic, Filamentous Bacte

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Bellilinea Caldifistulae Gen. Nov., Sp. Nov. and Longilinea Arvoryzae Gen. Nov., Sp. Nov., Strictly Anaerobic, Filamentous Bacte International Journal of Systematic and Evolutionary Microbiology (2007), 57, 2299–2306 DOI 10.1099/ijs.0.65098-0 Bellilinea caldifistulae gen. nov., sp. nov. and Longilinea arvoryzae gen. nov., sp. nov., strictly anaerobic, filamentous bacteria of the phylum Chloroflexi isolated from methanogenic propionate-degrading consortia Takeshi Yamada,1,2 Hiroyuki Imachi,2,3 Akiyoshi Ohashi,2 Hideki Harada,2,4 Satoshi Hanada,1 Yoichi Kamagata1,2,5 and Yuji Sekiguchi1,2 Correspondence 1Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science Yuji Sekiguchi and Technology (AIST), Tsukuba, Ibaraki 305-8566, Japan [email protected] 2Department of Environmental Systems Engineering, Nagaoka University of Technology, Nagaoka, Niigata 940-2188, Japan 3Subground Animalcule Retrieval Program, Extremobiosphere Research Center, Japan Agency for Marine-Earth Science & Technology (JAMSTEC), Yokosuka, Kanagawa 237-0061, Japan 4Department of Civil Engineering, Tohoku University, Sendai, Miyagi 980-8579, Japan 5Research Institute of Genome-based Biofactory, National Institute of Advanced Industrial Science and Technology (AIST), Sapporo, Hokkaido 062-8517, Japan Thermophilic (strain GOMI-1T) and mesophilic (strain KOME-1T) strains were isolated from two different cultures of propionate-degrading consortia obtained from thermophilic digester sludge and rice paddy soil, respectively. The two strains were non-spore-forming, non-motile and Gram-negative. Both strains were obligately anaerobic micro-organisms, showing multicellular filamentous morphotypes more than 100 mm in length. The cell width for strain GOMI-1T was 0.2–0.4 mm and that of strain KOME-1T was 0.4–0.6 mm. Strain GOMI-1T could grow at 45–65 6C with a pH range of 6.0–7.5 (optimum growth at 55 6C, pH 7.0). The temperature range for growth of strain KOME-1T was 30–40 6C and the pH range was pH 5.0–8.5 (optimum growth around 37 6C, pH 7.0). Yeast extract was required for growth of both strains. Strain GOMI-1T was able to grow with a number of carbohydrates in the presence of yeast extract. In yeast extract-containing medium, strain KOME-1T could utilize proteins and a limited range of sugars for growth. The G+C contents of the DNA of strains GOMI-1T and KOME-1T were T respectively 54.7 and 57.6 mol%. Major fatty acids of strain GOMI-1 were C16 : 0,C14 : 0 and T iso-C15 : 0, whereas those of strain KOME-1 were iso-C15 : 0, anteiso-C15 : 0 and C14 : 0. Based on comparative analysis of 16S rRNA gene sequences of strains GOMI-1T and KOME-1T, the strains were placed in different phylogenetic positions in the class Anaerolineae of the bacterial phylum Chloroflexi. Their phenotypic and genetic traits strongly supported the conclusion that the strains should be described as two independent taxa in the class Anaerolineae. Hence, we propose the names Bellilinea caldifistulae gen. nov., sp. nov., and Longilinea arvoryzae gen. nov., sp. nov., for strains GOMI-1T and KOME-1T. The type strains of Bellilinea caldifistulae and Longilinea arvoryzae are respectively GOMI-1T (5JCM 13669T 5DSM 17877T) and KOME-1T (5JCM 13670T 5KTCC 5380T). The class Anaerolineae has recently been proposed as a Abbreviations: NTA, nitrilotriacetate; UASB, upflow anaerobic sludge subclade in the phylum Chloroflexi with the related new blanket. class Caldilineae (Yamada et al., 2006). Analyses based on The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA sequences of 16S rRNA and the 16S rRNA gene have gene sequences of strains GOMI-1T and KOME-1T are respectively revealed that members of this class are distributed widely AB243672 and AB243673. in various types of ecosystems, such as the subsurface, Downloaded from www.microbiologyresearch.org by 65098 G 2007 IUMS Printed in Great Britain 2299 IP: 52.0.234.91 On: Tue, 16 Jul 2019 06:27:14 T. Yamada and others sediments, hot springs and aerobic and anaerobic sludge from the cultures, we first transferred part of the enrich- (Bjo¨rnsson et al., 2002; Hugenholtz et al., 1998a; Kindaichi ments to a fresh medium supplemented with sucrose et al., 2004; Sekiguchi et al., 1998; Teske et al., 2002), (20 mM) and yeast extract (0.1 %), because species of suggesting their ubiquity and functional significance in the Anaerolineae are commonly known as saccharolytic such environments (Hugenholtz et al., 1998b). However, anaerobes that require yeast extract. The medium used for the Anaerolineae have long been considered a group of the isolation and cultivation of the filamentous bacteria was yet-to-be-cultured microbes that are recalcitrant to cul- prepared as described previously (Sekiguchi et al., 2000; tivation and isolation (Hugenholtz et al., 1998b; Sekiguchi Yamada et al., 2005). Primary enrichment cultures et al., 2001). Recently, the first tangible micro-organism of inoculated with thermophilic digester sludge and rice the class was isolated and named Anaerolinea thermophila paddy soil were cultivated anaerobically at 55 uC and (Sekiguchi et al., 2001, 2003). In addition, three filamentous 37 uC, respectively. A number of successive transfers to strains belonging to the class (representing Anaerolinea fresh sucrose-yeast extract medium were conducted, and thermolimosa, Levilinea saccharolytica and Leptolinea tardivi- stable cultures that consisted mainly of the filamentous talis) were further isolated and characterized (Yamada et al., cells were finally established. Two strains, GOMI-1T and 2005, 2006). So far, these four strains are the only known KOME-1T, were isolated from these enriched cultures by organisms able to be cultivated and thoroughly described in the roll-tube isolation method (Hungate, 1969) with the class Anaerolineae. They are strictly anaerobic, multi- sucrose-yeast extract medium supplemented with purified cellular filamentous microbes and can utilize a number of agar (20 g agar noble l21; Difco). Isolation of strains carbohydrates fermentatively in the presence of yeast extract GOMI-1T and KOME-1T was performed at 55 uC and (Sekiguchi et al., 2001, 2003; Yamada et al., 2005, 2006). 37 uC, respectively. Tiny, colourless, lens-shaped colonies, Some of the strains require syntrophic association with a 0.1–0.2 mm in diameter, were formed within 1 month of hydrogenotrophic methanogen for efficient growth cultivation in both cases. (Sekiguchi et al., 2001, 2003; Yamada et al., 2005, 2006). For microscope observations, agar-coated slides were pre- To date, all authentic species of the Anaerolineae have been pared and microbial cells were immobilized on the slides initially found in and isolated from a special wastewater (Pfennig & Wagener, 1986). Both strains (strains GOMI-1T treatment system operating under anaerobic conditions and KOME-1T) showed flexible filaments of indefinite called the upflow anaerobic sludge blanket (UASB) system. length (generally longer than 100 mm) under the micro- However, besides the UASB system, there are many anaero- scope (Olympus AX80T) (Fig. 1). Cell widths of strains bic ecosystems in natural and artificial environments, and GOMI-1T and KOME-1T were respectively 0.2–0.4 mm and it is quite likely that an enormous number of unknown 0.4–0.6 mm (Fig. 1). Gram-staining done according to species of the Anaerolineae are hidden in such environ- Hucker’s method (Doetsch, 1981) was negative for both ments. We therefore searched anaerobic environments strains. Spore formation was not observed in either strain other than UASB sludges for novel species of the under any culture conditions. Gliding motility was not Anaerolineae. As a result, we successfully isolated two observed (based on the observation of colony forms on Anaerolineae-type filamentous anaerobes, designated strains solid agar medium). GOMI-1T and KOME-1T, from a thermophilic digester Strains GOMI-1T and KOME-1T were obligately anaerobic, sludge and rice paddy soil, respectively. In this report, the filamentous micro-organisms. Neither aerobic nor photo- isolation and detailed morphological, physiological and trophic growth in PE medium was observed in either strain chemotaxonomic characteristics and genetic features of the (Hanada et al., 1995). The following physiological tests, strains are described, assigning taxonomic placements to nutritional properties, usage of electron acceptors, fer- the strains in the class Anaerolineae. mentative end products and acid formation, were done The two filamentous strains were isolated from thermo- according to methods described previously (Imachi et al., philic (55 uC) and mesophilic (37 uC) methanogenic 2000, 2002; Roden & Lovley, 1993; Sekiguchi et al., 2000; propionate-degrading consortia enriched from thermo- Yamada et al., 2005). A small amount of yeast extract was philic digester sludge (55 uC) and rice paddy soil, respec- required for growth in both strains. In the presence of tively. Both consortia contained propionate-degrading yeast extract (0.01 %), strain GOMI-1T could utilize Pelotomaculum spp. and hydrogenotrophic methanogens the following substrates (20 mM each unless specified (Imachi et al., 2006). Besides these organisms, various otherwise): ribose, arabinose, fructose, glucose, galactose, morphotypes such as ovals, rods or filaments were mannose, sucrose, raffinose and pectin (5 g l21). The observed in the enrichment cultures. Fluorescence in situ following substrates supported weak growth of strain hybridization using the Chloroflexi-specific probe GOMI-1T and caused acid formation in medium supple- GNSB941* (Yamada et al., 2005) was performed according mented with yeast extract
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