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Halorubrum Halophilum Sp. Nov., an Extremely Halophilic Archaeon Isolated from a Salt-Fermented Seafood

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Halorubrum Halophilum Sp. Nov., an Extremely Halophilic Archaeon Isolated from a Salt-Fermented Seafood Antonie van Leeuwenhoek (2014) 105:603–612 DOI 10.1007/s10482-014-0115-6 ORIGINAL PAPER Halorubrum halophilum sp. nov., an extremely halophilic archaeon isolated from a salt-fermented seafood Kyung June Yim • In-Tae Cha • Hae-Won Lee • Hye Seon Song • Kil-Nam Kim • Sung-Jae Lee • Young-Do Nam • Dong-Wook Hyun • Jin-Woo Bae • Sung-Keun Rhee • Myung-Ji Seo • Jong-Soon Choi • Hak-Jong Choi • Seong Woon Roh • Daekyung Kim Received: 21 August 2013 / Accepted: 7 January 2014 / Published online: 18 January 2014 Ó Springer Science+Business Media Dordrecht 2014 Abstract A novel, red-pigmented, pleomorphic and catalase and oxidase activities were found to be short rod-shaped haloarchaeon, designated B8T, was positive and nitrate was reduced in aerobic conditions. isolated from a salt-fermented seafood. Strain B8T was Tween 20, 40 and 80 were found to be hydrolyzed, found to be able to grow at 20–45 °C, in the presence of whereas casein, gelatin and starch were not hydro- 15–30 % (w/v) NaCl and at pH 7.0–9.0. The optimum lyzed. Indole or H2S was not formed and urease activity requirements were found to be a temperature range of was not detected. A phylogenetic analysis based on the 35–40 °C, pH 8.0 and the presence of 25 % NaCl. The 16S rRNA gene sequences indicated that strain B8T is cells of strain B8T were observed to be Gram-staining most closely related to members of the genus Haloru- negative and lysed in distilled water. Anaerobic growth brum in the family Halobacteriaceae. Strain B8T was did not occur in the presence of nitrate, L-arginine, found to have three 16S rRNA genes, rrnA, rrnB and dimethyl sulfoxide or trimethylamine N-oxide. The rrnC; similarities between the 16S rRNA gene sequences are 99.0–99.8 %. Strain B8T shared 99.0 % 16S rRNA gene sequence similarity with Kyung June Yim and In-Tae Cha have contributed equally to Halorubrum (Hrr.) lipolyticum JCM 13559T and Hrr. this work. saccharovorum DSM 1137T, 98.8 % with Hrr. kocurii T Electronic supplementary material The online version of JCM 14978 , 98.3 % with Hrr. lacusprofundi DSM T T this article (doi:10.1007/s10482-014-0115-6) contains supple- 5036 , 98.0 % with Hrr. arcis JCM 13916 , 97.7 % mentary material, which is available to authorized users. K. J. Yim Á I.-T. Cha Á H.-W. Lee Á H. S.-J. Lee Á D.-W. Hyun Á J.-W. Bae S. Song Á K.-N. Kim Á S. W. Roh (&) Á D. Kim (&) Department of Life and Nanopharmaceutical Sciences and Jeju Center, Korea Basic Science Institute, Jeju 690-140, Department of Biology, Kyung Hee University, Seoul Republic of Korea 130-701, Republic of Korea e-mail: [email protected] Y.-D. Nam D. Kim Fermentation and Functionality Research Group, Korea e-mail: [email protected] Food Research Institute, Sungnam 463-746, Republic of Korea I.-T. Cha Á S.-K. Rhee Department of Microbiology, Chungbuk National M.-J. Seo University, Cheongju 361-763, Republic of Korea Division of Bioengineering, Incheon National University, Incheon 406-772, Republic of Korea H.-W. Lee Á H.-J. Choi World Institute of Kimchi, Gwangju 503-360, Republic of Korea 123 604 Antonie van Leeuwenhoek (2014) 105:603–612 with Hrr. aidingense JCM 13560T and 97.0 % with Nomenclature (Euze´by 1997). In particular, the genus Hrr. aquaticum JCM 14031T, as well as 93.7–96.5 % Halorubrum, which was proposed formally by McGe- with other type strains in the genus Halorubrum. The nity and Grant (1995), currently includes 25 validly RNA polymerase subunit B0 gene sequence similarity named species: Halorubrum (Hrr.) aidingense (Cui of strain B8T with Hrr. kocurii JCM 14978T is 97.2 % et al. 2006), Hrr. alkaliphilum (Feng et al. 2005), Hrr. and lower with other members of the genus Haloru- aquaticum (Gutie´rrez et al. 2011), Hrr. arcis (Xu et al. brum. DNA–DNA hybridization experiments showed 2007), Hrr. californiense (Pesenti et al. 2008), Hrr. that strain B8T shared equal or lower than 50 % chaoviator (Mancinelli et al. 2009), Hrr. cibi (Roh and relatedness with reference species in the genus Ha- Bae 2009), Hrr. coriense (Oren and Ventosa 1996), Hrr. lorubrum. The genomic DNA G?C content of strain distributum (Oren and Ventosa 1996), Hrr. ejinorense B8T was determined to be 64.6 mol%. The major (Castillo et al. 2007), Hrr. ezzenmoulense (Kharroub isoprenoid quinone of strain B8T was identified as et al. 2006), Hrr. kocurii (Gutie´rrez et al. 2008), Hrr. menaquinone-8 and the major polar lipids as phos- lacusprofundi (McGenity and Grant 1995), Hrr. lipo- phatidylglycerol, phosphatidylglycerol phosphate lyticum (Cui et al. 2006), Hrr. litoreum (Cui et al. 2007), methyl ester, phosphatidylglycerol sulfate, sulfated Hrr. luteum (Hu et al. 2008), Hrr. orientale (Castillo mannosyl glucosyl diether and an unidentified et al. 2006), Hrr. saccharovorum (Tomlinson and phospholipid. Based on this polyphasic taxonomic Hochstein 1976;McGenityandGrant1995), Hrr. study, strain B8T is considered to represent a new sodomense (McGenity and Grant 1995), Hrr. tebenqui- species in the genus Halorubrum, for which the name chense (Lizama et al. 2002), Hrr. terrestre (Ventosa Hrr. halophilum sp. nov. is proposed. The type strain is et al. 2004), Hrr. tibetense (Fan et al. 2004), Hrr. B8T (=JCM 18963T = CECT 8278T). trapanicum (McGenity and Grant 1995), Hrr. vacuol- atum (Mwatha and Grant 1993;Kamekuraetal.1997) Keywords Haloarchaea Á Halorubrum and Hrr. xinjiangense (Feng et al. 2004). Cells of the halophilum Á Polyphasic taxonomy Á genus Halorubrum are rods or irregular-shaped, motile Salt-fermented seafood or non-motile, strictly aerobic and oxidase and catalase- positive. The major polar lipids are phosphatidylglyc- erol (PG), phosphatidylglycerol phosphate methyl ester Introduction (PGP-Me), phosphatidylglycerol sulfate (PGS) and/or sulfated mannosyl glucosyl diether (S-DGD-3) (McGe- High salinity is toxic to most cells but many extremely nity and Grant 1995). The G?C content of the genomic halophilic archaea, i.e. haloarchaea, have been isolated DNA is in the range of 61.7–71.2 mol% (McGenity and in hypersaline environments (Grant 2004). Well known Grant 2001; Roh and Bae 2009). The present study hypersaline environments for the isolation of haloar- characterized a new haloarchaeon, strain B8T and chaea are soda lakes, salt lakes and solar salterns, but determined the taxonomic position of this strain based some haloarchaea have been isolated from a salt- on phenotypic, phylogenetic and chemotaxonomic fermented seafood made from shrimp (Roh et al. 2007a, analyses, according to the proposed minimal standards b, 2009; Roh and Bae 2009). All haloarchaea are for the description of new taxa in the order Halobac- classified within the family Halobacteriaceae in the teriales (Oren et al. 1997). Based on this polyphasic order Halobacteriales of the phylum Euryarchaeota. taxonomic study, strain B8T is considered to represent a This family currently contains 40 genera based on the new species in the genus Halorubrum, for which the List of Prokaryotic Names with Standing in name Hrr. halophilum sp. nov. is proposed here. J.-S. Choi Division of Life Science, Korea Basic Science Institute, Materials and methods Daejeon 305-806, Republic of Korea J.-S. Choi Archaeal strain and culture conditions Graduate School of Analytical Science and Technology, Chungnam National University, Daejeon 305-764, A strain, designated B8T, was isolated from a salt- Republic of Korea fermented seafood made from shrimp. A sample was 123 Antonie van Leeuwenhoek (2014) 105:603–612 605 serially diluted and spread onto a complex medium described by Benson (2002) using medium 954 as the (DSM medium no. 954), which was adjusted to pH 7.0 basal medium. The hydrolysis of Tween 20, 40 and 80 and contained the following (l-1): 5 g casamino acids were tested as described by Gonza´lez et al. (1978) and (BD), 5 g yeast extract (BD), 20 g MgCl2Á6H2O, 2 g the hydrolysis of gelatin was tested according to KCl, 12 g Tris, 0.2 g CaCl2Á2H2O, and 200 g NaCl. A Smibert and Krieg (1994) using medium 954 as the solid medium was prepared by adding 2 % (w/v) agar. basal medium. Anaerobic growth was tested in filled, A single colony was streaked repeatedly to obtain a stoppered tubes using medium 954 in the presence of pure culture at 37 °C. For long-term preservation, 30 mM nitrate, 5 g L-arginine, 5 g DMSO or 5 g strain B8T was frozen at -80 °C in medium 954 trimethylamine N-oxide (TMAO) at 37 °Cinan supplemented with 5 % (v/v) dimethyl sulfoxide anaerobic chamber (Coy), where the atmosphere T (DMSO). Hrr. lipolyticum JCM 13559 , Hrr. kocurii comprised N2/CO2/H2 (90:5:5, by vol.). H2S forma- JCM 14978T, Hrr. saccharovorum DSM 1137T, Hrr. tion was tested according to Cui et al. (2007). Acid T lacusprofundi DSM 5036 Hrr. aidingense JCM production from D-glucose was tested by growing T T T 13560 , Hrr. arcis JCM 13916 and Hrr. aquaticum strain B8 in HMD supplemented with 1 % D-glucose. JCM 14031T were obtained from Deutsche Sammlung Methyl red and Voges–Proskauer tests were deter- von Mikroorganismen und Zellkulturen GmbH mined using MR-VP Broth (BD) and Simmon’s citrate (DSMZ) or Japan Collection of Microorganisms test was performed using Simmons citrate agar (DB), (JCM) and used in the comparative taxonomic for which each medium was supplemented with 20 % analyses. (w/v) NaCl. Arginine, lysine and ornithine decarbox- ylases tests were carried out using Moeller Decarbox- Morphological, physiological and biochemical ylase Broth Base (BD) containing 20 % (w/v) NaCl as characterization the basal medium. To assess the utilization of sole carbon and energy sources, HMD was supplemented All of the phenotypic tests were performed using with 10 mM bis–Tris propane and 1 % of the follow- medium 954 or a halophile medium (HMD) that ing substrates: acetate, L-alanine, L-arginine, L-aspar- -1 contained (l ): 20 g MgCl2Á6H2O, 5 g K2SO4, 0.1 g tate, citrate, D-fructose, fumarate, D-galactose, D- CaCl2Á2H2O, 0.1 g yeast extract, 0.5 g NH4Cl, 0.05 g glucose, L-glutamate, glycerol, glycine, DL-lactate, KH2PO4, 0.5 g casamino acids as a carbon source and lactose, L-lysine, L-malate, maltose, mannitol, D-man- 180 g NaCl (Savage et al.
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