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Lactivibrio Alcoholicus Gen. Nov., Sp. Nov., an Anaerobic, Mesophilic, Lactate-, Alcohol-, Carbohydrate- and Amino-Acid-Degradin

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Lactivibrio Alcoholicus Gen. Nov., Sp. Nov., an Anaerobic, Mesophilic, Lactate-, Alcohol-, Carbohydrate- and Amino-Acid-Degradin International Journal of Systematic and Evolutionary Microbiology (2014), 64, 2137–2145 DOI 10.1099/ijs.0.060681-0 Lactivibrio alcoholicus gen. nov., sp. nov., an anaerobic, mesophilic, lactate-, alcohol-, carbohydrate- and amino-acid-degrading bacterium in the phylum Synergistetes Yan-Ling Qiu,1,2 Satoshi Hanada,3 Yoichi Kamagata,4 Rong-Bo Guo1 and Yuji Sekiguchi2 Correspondence 1Shandong Industrial Engineering Laboratory of Biogas Production & Utilization, Yan-Ling Qiu Key Laboratory of Biofuels, Qingdao Institute of Bioenergy and Bioprocess Technology, [email protected] Chinese Academy of Sciences, Qingdao, Shandong Province 266101, PR China 2Biomedical Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Ibaraki 305-8566, Japan 3Bioprocess Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Ibaraki 305-8566, Japan 4Bioprocess Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Sapporo, Hokkaido 062-8517, Japan A mesophilic, obligately anaerobic, lactate-, alcohol-, carbohydrate- and amino-acid- degrading bacterium, designated strain 7WAY-8-7T, was isolated from an upflow anaerobic sludge blanket reactor treating high-strength organic wastewater from isomerized sugar production processes. Cells of strain 7WAY-8-7T were motile, curved rods (0.7–1.0¾5.0–8.0 mm). Spore formation was not observed. The strain grew optimally at 37 6C (range for growth was 25–40 6C) and pH 7.0 (pH 6.0–7.5), and could grow fermentatively on yeast extract, glucose, ribose, xylose, malate, tryptone, pyruvate, fumarate, Casamino acids, serine and cysteine. The main end-products of glucose fermentation were acetate and hydrogen. In co-culture with the hydrogenotrophic methanogen Methanospirillum hungatei DSM 864T, strain 7WAY-8-7T could utilize lactate, glycerol, ethanol, 1-propanol, 1-butanol, L-glutamate, alanine, leucine, isoleucine, valine, histidine, asparagine, glutamine, arginine, lysine, threonine, 2-oxoglutarate, aspartate and methionine. A Stickland reaction was not observed with some pairs of amino acids. Yeast extract was required for growth. Nitrate, sulfate, thiosulfate, elemental sulfur, sulfite and Fe (III) were not used as terminal electron acceptors. The G+C content of the genomic DNA was 61.4 mol%. 16S rRNA gene sequence analysis revealed that the isolate belongs to the uncultured environmental clone clade (called ‘PD-UASB-13’ in the Greengenes database) in the bacterial phylum Synergistetes, showing less than 90 % sequence similarity with closely related described species such as Aminivibrio pyruvatiphilus and Aminobacterium colombiense (89.7 % and 88.7 %, respectively). The major cellular fatty acids were iso-C13 : 0, iso-C15 : 0, anteiso-C15 : 0,C18 : 1,C19 : 1,C20 : 1 and C21 : 1. A novel genus and species, Lactivibrio alcoholicus gen. nov., sp. nov. is proposed to accommodate strain 7WAY-8-7T (5JCM 17151T5DSM 24196T5CGMCC 1.5159T). The bacterial phylum Synergistetes was proposed recently, ‘subdivision A’ has been formally described as the class being subdivided into five major lines of descent as order- Synergistia (Jumas-Bilak et al., 2009). Based on culture- level lineages (i.e. ‘subdivisions A–E’), of which only dependent and culture-independent surveys, members of the phylum Synergistetes have been found in a wide range Abbreviations: FAME, fatty acid methyl ester; UASB, upflow anaerobic of anoxic ecosystems, such as anaerobic wastewater treat- sludge blanket. ment systems, soil, and gastrointestinal tracts (Vartoukian The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene et al., 2007). Members of this phylum have also been found sequence of strain 7WAY-8-7T is AB558582. in specimens from periodontal disease, gastrointestinal One supplementary figure is available with the online version of this paper. infections, genital tract and soft tissue infections, suggesting 060681 G 2014 IUMS Printed in Great Britain 2137 Y.-L. Qiu and others that members of the phylum play a possible pathogenic role Greengenes database; McDonald et al., 2012) in the phylum (Horz et al., 2006; Vartoukian et al., 2007). Synergistetes ‘subdivision E’. Despite its habitat diversity, cultured strains representing Strain 7WAY-8-7T was originally obtained from the the phylum Synergistetes characterized to date largely share granular sludge of a mesophilic (35 uC) full-scale upflow similar phenotypic traits with one another. To date, thirteen anaerobic sludge blanket reactor (UASB) treating a high- genera with twenty-two species with validly published strength organic wastewater from isomerized sugar pro- names have been cultivated and characterized in the phylum duction processes (Narihiro et al., 2009). The medium used Synergistetes: all of the described species within this phylum for isolation and cultivation was prepared as described are strictly anaerobic, neutrophilic, Gram-negative rods that previously (Sekiguchi et al., 2000). Gently washed and (mostly) specifically ferment amino acids. The characteristic homogenized sludge was serially diluted 10-fold in anaer- of amino acid fermentation is also supported by represent- obic liquid medium supplemented with low concentrations ative genomes of members of the phylum Synergistetes, for of acetate (1 mM) and yeast extract (0.01 %, w/v) and which a greater average proportion of amino acid transport pH 7.0. Growth of cells was observed in the 1028 dilution and metabolism genes (COG functional category E) has tube after 1 month of incubation at 37 uC. Cells in the been predicted than for any bacterial phylum to date highest dilution were further purified by repeated serial (Hugenholtz et al., 2009). Carbohydrate fermentation dilution in glucose (1 mM) and yeast extract (0.01 %, w/v) is exceptionally exhibited by a few cultured species in medium, and then in the same agar roll tubes (2 %, w/v; the phylum Synergistetes, such as Thermanaerovibrio velox Difco Noble agar). Small, light brown, lens-shaped colonies, (Zavarzina et al., 2000) and Anaerobaculum spp. (Rees et al., were formed after 2–3 weeks of incubation at 37 uC. This 1997; Menes & Muxı´, 2002). These observations based on roll tube isolation step (transferring single colonies from cultured members of the phylum Synergistetes suggested solid medium to liquid medium) was repeated several times that members of the phylum are specialists with relatively and a purified strain, designated strain 7WAY-8-7T was shallow ecophysiological niches (Godon et al., 2005). obtained. However, recent cultivation and culture-independent studies Cell morphology was examined under a fluorescent micro- are highlighting the presence of more versatile metabolic scope (Olympus BX50F). Transmission electron micro- capabilities of members of the phylum Synergistetes.Recently, scopy was performed with a Hitachi H-7000 transmission a novel rumen bacterium within the phylum Synergistetes was electron microscope as described previously (Sekiguchi described that metabolizes fluoroacetate under anaerobic et al., 2003). The Gram staining reaction was performed by conditions, indicating the presence of reductive dehalogena- the method of Hucker (Doetsch, 1981). Cells were motile, tion capability for growth in the phylum Synergistetes (Davis curved rods, 0.7–1.0 mm wide and 5.0–8.0 mm in length et al., 2012). In addition, Delbe`s et al. (2001) reported a (Fig. 1). Cells became spirilloid in ageing cultures. Cells as marked increase in 16S rRNA of uncultured members of long as 15.0 mm were observed. Spore formation was not the phylum Synergistetes (AA56) following the addition of observed and Gram-staining was negative. lactate under anoxic conditions, indicating the involvement The physiological traits of strain 7WAY-8-7T were examined of members of the phylum Synergistetes in anaerobic lactate as described previously (Sekiguchi et al., 2000). Growth was degradation. Ito et al. (2011) suggested that an uncultured determined at 20–55 uC (at intervals of 5 uC), at pH 5.0–8.5 group of the phylum Synergistetes (named ‘Synergistes group (at intervals of 0.5 pH unit; 37 uC) and with 0–3.0 % (w/v) 4 anaerobic digester’) was one of the major acetate-utilizing NaCl (at intervals of 0.5 %). The growth of cells was taxa in an anaerobic digester, presumably indicating its evaluated on the basis of the increase in optical density at syntrophic acetate-oxidation capability with hydrogeno- 400 nm and the production of hydrogen. Unless otherwise trophic methanogens. However, no cultured strains repre- indicated, the organism was cultured anaerobically (N / senting the phylum Synergistetes capable of performing such 2 CO , 80 : 20, v/v) at 37 uC without shaking. Aerobic growth metabolism have been obtained so far, hampering further 2 was tested in a medium containing 2 mM glucose and confirmation of these additional metabolic traits of the 0.01 % (w/v) yeast extract under aerobic conditions without phylum Synergistetes. the addition of reducing agents. Strain 7WAY-8-7T grew To further explore and confirm the ecophysiological roles of anaerobically on glucose/yeast extract medium after 8 weeks members of the phylum Synergistetes besides amino acid of incubation at 25–40 uC (optimum, 37 uC), at pH 6.0–7.5 fermentation, we aimed at isolating members of the phylum (optimum, approximately pH 7.0) and with 0–2.0 % (w/v) Synergistetes that exhibit broader metabolic capabilities. NaCl, but did not grow at temperatures below 25 uCor Through these attempts,
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