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Haloarcula Quadrata Sp. Nov., a Square, Motile Archaeon Isolated from a Brine Pool in Sinai (Egypt)

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Haloarcula Quadrata Sp. Nov., a Square, Motile Archaeon Isolated from a Brine Pool in Sinai (Egypt) International Journal of Systematic Bacteriology (1999), 49, 1 149-1 155 Printed in Great Britain Haloarcula quadrata sp. nov., a square, motile archaeon isolated from a brine pool in Sinai (Egypt) Aharon Oren,’ Antonio Ventosa,2 M. Carmen Gutierrez* and Masahiro Kamekura3 Author for correspondence: Aharon Oren. Tel: +972 2 6584951. Fax: +972 2 6528008. e-mail : orena @ shum.cc. huji. ac.il 1 Division of Microbial and The motile, predominantly square-shaped, red archaeon strain 80103O/lT, Molecular Ecology, isolated from a brine pool in the Sinai peninsula (Egypt), was characterized Institute of Life Sciences and the Moshe Shilo taxonomically. On the basis of its polar lipid composition, the nucleotide Center for Marine sequences of its two 16s rRNA genes, the DNA G+C content (60-1 molo/o) and its Biogeochemistry, The growth characteristics, the isolate could be assigned to the genus Haloarcula. Hebrew University of Jerusalem, Jerusalem However, phylogenetic analysis of the two 165 rRNA genes detected in this 91904, Israel organism and low DNA-DNA hybridization values with related Haloarcula 2 Department of species showed that strain 801030/ITis sufficiently different from the Microbiology and recognized Haloarcula species to warrant its designation as a new species. A Parasitology, Faculty of new species, Haloarcula quadrata, is therefore proposed, with strain 801030/IT Pharmacy, University of SeviIIe, SeviIIe 41012, Spain (= DSM 119273 as the type strain. 3 Noda Institute for Scientific Research, 399 Noda, Noda-shi, Chiba-ken Keywords : Haloarcula quadrata, square bacteria, archaea, halophile 278-0037, Japan INTRODUCTION this type of bacterium from a Spanish saltern was published by Torrella (1986). Unfortunately, this Square bacteria were first observed in 1980 by Walsby isolate has not been deposited in a culture collection in the Gavish Sabkha, a coastal brine pool in the Sinai and the culture was lost many years ago. Other peninsula, Egypt (Parkes & Walsby, 1981 ; Walsby, attempts to isolate this intriguing type of prokaryote 1980). Walsby recognized these extremely thin, square- from a variety of hypersaline environments (the Gavish shaped structures as prokaryotes due to the presence Sabkha, salterns of Guerrero Negro, Baja California of refractile gas vacuoles. Square bacteria have since and San Diego, California) led to the isolation of ‘ box- been reported to occur in many thalassohaline hyper- shaped ’ pleomorphic red halophilic archaea, lacking saline environments in which the salt concentration gas vacuoles, which were classified in the genus exceeds 200-250 g l-l, and up to NaCl saturation. Haloarcula on the basis of their polar lipid composition These include saltern crystallizer ponds in Israel (Oren, and 16s rRNA nucleotide sequences. These strains 1994; Oren et al., 1996), Spain (Guixa-Boixareu et al., (species incertae sedis ‘ Haloarcula sinaiiensis ’ and 1996; Torrella, 1986), San Francisco Bay (USA) and ‘Haloarcula californiae’) (Javor et al., 1982) still await Baja California (Mexico) (Javor et al., 1982; a more detailed characterization in order to define Stoeckenius, 1981). their taxonomic position. The triangular and rhom- boid cells of Haloarcula japonica (Takashina et al., The gas-vacuole-containing type of square bacteria 1990) show some morphological similarity to these observed by Walsby has never been obtained in isolates. culture. A single report of the successful isolation of Early isolation experiments yielded a motile, square .. .. .. I.. .. I.. .. .I.. bacterium from the Gavish Sabkha. This strain, which Abbreviations: PG, PGP, PGS, the diether derivatives of phospha- IT. tidylglycerol, the methyl ester of phosphatidylglycerophosphate and lacks gas vacuoles, was designated 801030/ Its phosphatidylglycerosulfate, respectively; TGD-2,l -O-[@-glucose-(l’ -+ 6’)- morphological characteristics and its interesting mode a-D-mannose-(I‘ -+ 2’)-a-~-gIucose]-2,3-di-O-phytanyI-sn-glyceroI. of motility were reported by Alam et al. (1984). Cells The DDBJ accession numbers for the 165 rRNA sequences of strain may possess a single flagellum or ’Several flagella 801030/lT are AB010964 and AB010965. anchored from a single or from several locations on the 00946 0 1999 IUMS 1149 A. Oren and others cell surface. Several filaments may form a stable bundle KC1, 0.373; CaC1, .2H,O, 0.5; MnCl,, 0.013 mg 1-l; and that does not fall apart when changing from clockwise yeast extract, 5 (pH 7). Other halophilic archaea used as to anti-clockwise movement and vice versa. Instead reference strains were grown in this medium or other suitable of the three flagellar proteins present in flagella of media, as required. The growth medium was modified with Halobacterium, respect to salt concentration, yeast extract content, addition SDS-PAGE of isolated flagella of of other nutrients, buffers, antibiotics, etc., as specified in the strain 801030/lT showed the presence of a single experiments. For growth experiments at different pH values, flagellin band with an apparent molecular mass of the buffers MES (in the pH range 59-55), PIPES (pH 6-7) 73 kDa. and HEPES (PH 7-5-9.0) were added at a final concentration of 25 mM. These strains were routinely grown with shaking We have performed a taxonomic characterization of at 35 "C in 100 or 250 ml Erlenmeyer flasks containing 30 or the square motile strain 801030/lT. On the basis of its 100 ml medium, respectively. Growth was assessed by growth characteristics, its polar lipid composition and measuring the OD,,, of the cultures. the nucleotide sequences of its 16s rRNA genes, the Phenotypic characterization.Unless specified otherwise, tests isolate could be assigned to the genus Haloarcula. for phenotypic properties were carried out as indicated in the However, based on phylogenetic analysis of the two proposed minimal standards for the description of new taxa different 16s rRNA genes detected in this organism in the order Halobacteriales (Oren et al., 1997). Degradation and the low DNA-DNA hybridization values with the of Tween and gelatin was tested as recommended by Gutikrrez & Gonzalez (1972). Appropriate positive and other Haloarcula species, the isolate is sufficiently negative controls were included in all tests performed. different from the recognized Haloarcula species to Formation of acids from different sugars was tested in media warrant its designation as a new species. in which the yeast extract concentration was reduced to 1.0 or 0.5 g l-', amended with 0.5 g NH,C1 1-1 and 5 g of the sugar tested 1-1 (autoclaved separately). To examine growth stimulation by sugars and other compounds, this medium METHODS was buffered at pH 7.0 by including 20 mM PIPES. To test for the ability of single carbon sources to support growth, Bacterial strains. A culture of isolate 801030/lT (Alam et at., yeast extract was omitted, and the compound to be tested 1984) was kindly supplied by M. Kessel (Bethesda, MD, was added at a concentration of 5 g l-l, together with 1 g USA). For comparison, reference strains of halophilic NH,C1 1-1 and 0-05 g KH,PO, 1-1 and 20 mM PIPES. The archaea were included in this study, as listed in Table 1. outcome was considered positive when growth was obtained in at least four successive transfers in this medium. Cultivation conditions. The standard growth medium used Growth and gas formation with nitrate as electron acceptor for strain 801030/lT and other Haloarcula strains (Oren et were tested in 100 ml glass-stoppered bottles completely al., 1988) contained (in g 1-l) : NaC1,206; MgSO,. 7H,O, 36; filled with growth medium to which 5 g NaNO, 1-1 was Table 7- DNA relatedness among strain 801030/lT and other halophilic archaea studied DNA-DNA relatedness values are mean results of at least three independent determinations, which generally did not differ by more that 5 YO.T, Type strain. Organism Percentage hybridization with 3H-labelled DNA from strain 801030/lT Haloarcula strain 801030/lT 100 Haloarcula vallismortis ATCC 2971 5T 20 Haloarcula marismortui ATCC 43049T < 10 Haloarcula hispanica ATCC 33960T 22 Haloarcula japonica JCM 7785T 34 Haloarcula argentinensis ATCC 2984 1 14 Haloarcula mukohataei DSM 1 1483T < 10 ' Haloarcula sinaiiensis' ATCC 33800 < 10 Haloferax gibbonsii ATCC 33959T 18 Haloferax volcanii NCIMB 2012T < 10 Haloferax mediterranei ATCC 33500T < 10 Halobacterium salinarum DSM 3754T 18 Halorubrum saccharovorum ATCC 29252T 15 Halorubrum lacusprofundi DSM 5036T < 10 Halorubrum sodomense ATCC 337ST < 10 Halorubrum distributum JCM 9 1OOT < 10 Halobaculum gomorrense DSM 9297T < 10 Natrialba asiatica JCM 957P < 10 1150 International Journal of Systematic Bacteriology 49 Haloarcula quadrata sp. nov. added and which included an inverted test tube to observe competitor to labelled DNA was at least 150: 1. The final the formation of gas. Anaerobic growth in the presence of volume and concentration were adjusted to 140 pl, 2 x SSC 5 g L-arginine. HC1 1-1 was tested in completely filled 25 ml and 30 Y formamide. Hybridization was performed for 18 h stoppered tubes. Controls without nitrate or arginine were in a water bath (Grant Instruments) with slow shaking at included and all incubations were performed in the dark. 56 "C, which is within the limits of validity for the filter Haloarcula marismortui was used as a positive control for method (De Ley & Tijtgat, 1970), in triplicate. After the formation of nitrite and gas from nitrate, and hybridization, the filters were washed in 2x SSC at the Halobacterium salinarum served as a positive control for optimal renaturation temperature (56 "C). The radioactivity anaerobic growth on arginine. bound to the filters was measured in a liquid scintillation Polar lipid characterization. Cell pellets from 20 ml culture counter (Beckman Instruments) and the percentage hom- were suspended in I m14 M NaCl and extracted with 3.75 ml ology was calculated according to Johnson (1994). At least methanol/chloroform (2: 1, v/v) for 4 h.
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