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Taxonomic Study of Extreme Halophilic Archaea Isolated from the “Salar De Atacama”, Chile

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Taxonomic Study of Extreme Halophilic Archaea Isolated from the “Salar De Atacama”, Chile System. Appl. Microbiol. 24, 464–474 (2001) © Urban & Fischer Verlag http://www.urbanfischer.de/journals/sam Taxonomic Study of Extreme Halophilic Archaea Isolated from the “Salar de Atacama”, Chile CATHERINE LIZAMA1,2, MERCEDES MONTEOLIVA-SÁNCHEZ1, BERNARDO PRADO2, ALBERTO RAMOS-CORMENZANA1, JURGEN WECKESSER3 and VICTORIANO CAMPOS2 1Department of Microbiology, Faculty of Pharmacy, University of Granada, Campus Universitario de Cartuja Granada, Spain 2Laboratory of Microbiology, Institute of Biology, Faculty of Basic and Mathematics Sciences, Catholic University of Valparaíso, Val- paraíso, Chile 3Institute of Biology and Microbiology, Freiburg, Germany Received July 1, 2001 Summary A large number of halophilic bacteria were isolated in 1984–1992 from the Atacama Saltern (North of Chile). For this study 82 strains of extreme halophilic archaea were selected. The characterization was performed by using the phenotypic characters including morphological, physiological, biochemical, nu- tritional and antimicrobial susceptibility test. The results, together with those from reference strains, were subjected to numerical analysis, using the Simple Matching (SSM) coefficient and clustered by the unweighted pair group method of association (UPGMA). Fifteen phena were obtained at an 70% simi- larity level. The results obtained reveal a high diversity among the halophilic archaea isolated. Represen- tative strains from the phena were chosen to determine their DNA base composition and the percentage of DNA-DNA similarity compared to reference strains. The 16S rRNA studies showed that some of these strains constitutes a new taxa of extreme halophilic archaea. Key words: Atacama Saltern – Tebenquiche Lake – Extreme Halophilic Archaea – Numerical Taxonomy Introduction The extreme halophilic archaea require at least 1.5 M promise of providing valuable molecules for biotechno- NaCl. Most strains grow best at 3.5–4.5 M NaCl. They logical use in industry (HORIKOSHI, 1997). have been isolated from different habitats including alka- In a previous study carried out on the Atacama saltern line and salt lakes, marine salterns, the Dead Sea and (MORAGA et al., 1974) was showed that the characteris- saline soils. Traditionally the family Halobacteriaceae tics of this habitat, in relation with geographic, climatic contains six genera: Halobacterium, Haloarcula, Halofer- ax, Halococcus and two alkalophilic genera, Natrono- bacterium and Natronococcus (HOLT et al., 1994). Re- Abbreviations: PG – phosphatidylglycerol (diether analogue); cently, applying molecular techniques nine new genera PGP – phosphatidylglycerolphosphate (diether analogue); PGS – were described: Halorubrum (MCGENITY et al., 1995), phosphatidylglycerolsulfate (diether analogue); S-DGD-1 – α → Halobaculum (OREN et al., 1995), Natrialba (KEMEKURA monosulphated diglycosylglyceroldiether (6-HSO3-Man p- 1 et al., 1995), Natronomonas (KAMEKRA et al., 1997), 2-Glc p-α1 → 1-glyceroldiether); DGD-1 – diglycosylglyc- α → α → Halogeometricum (MONTALVO-RÓDRIGUEZ et al., 1998), eroldietther (Man p- 1 2-Glc p- 1 1-glyceroldiether); S-DGD-3 – monosulphated diglycosylglyceroldiether (2-HSO - Natrinema (MCGENETY et al., 1998), Haloterrigena 3 Man p-α1 → 2-Glc p-α1 → 1-glyceroldiether); S-TGD-1 – sul- (VENTOSA et al., 1999), Natronorubrum (XU et al., 1999) β → fated triglycosylglyceroldiether (3-HSO3-Gal p- -1 6-Man and Halorhabdus (WAINØ et al., 2000) extending the di- p-α1 → 2-Glc p-α1- glyceroldiether); TGD-1 – triglycosylglyc- versity of the taxonomy of halophilic archaea. Halophilic eroldiether (Gal p-β-1 → 6-Man p-α1 → 2-Glc p-α1- glyc- microorganisms offer important insights into the biology eroldiether); TGD-2 – triglycosylglyceroldiether (Glc p-β-1 → and evolution of many organisms and also hold the 6-Man p-α1 → 2-Glc p-α1- glyceroldiether). 0723-2020/01/24/03-464 $ 15.00/0 Extreme halophilic archaea from “Salar de Atacama” 465 and chemical composition, revealed it to be an ideal envi- For the nutritional test, a modified minimal medium de- ronment for the development of extreme halophilic mi- scribed by RODRÍGUEZ-VALERA et al. (1980), was used: 20% croorganisms. In previous works were showed new iso- (w/v) total salts; 0.2% NH4Cl and 0.1% KH2PO4. The pH was lates of moderately halophilic microrganisms as gram- adjusted to 7.0 with NaOH 4 M. The media was filtered before sterilization. The substrates were used in the following concen- negative rods (PRADO et al., 1991) as well as gram posi- trations: 0.2% for carbohydrates, and 0.1% for alcohols and or- tive cocci (VALDERRAMA et al., 1991). The purpose of this ganic acids. The media were sterilized by heating at 90 ºC for 15 study was to widens the knowledge of the biodiversity of minutes. For all the tests, inocula with young bacterial suspen- extremely halophilic archaea on the Atacama saltern . sions were used and maintained for 24 h. in saline solutions, in order to eliminate possible nutritional reserves that could be cause erroneous results. Minimal media without substrate and Materials and Methods media HE at 25% (w/v) total salts were used as controls. Tur- bidity of the positive tubes was determined after seven days of Isolation and culture conditions incubation at 40 ºC. The 82 strains studied were isolated from water and sedi- The utilization of amino acids as carbon and nitrogen ment of Lake Tebenquiche, located in the northern part of Ata- sources was determined using the method described previously cama Saltern, and from the sediment of Poligonal Zone. Water by VENTOSA et al. (1982), with a basal medium in which was samples of 100, 50 and 10 ml were filtered in situ using special deleted the inorganic nitrogen sources. The composition was as membranes (Sartorius 11406/0.45/324/1) which were placed on follows (g/l): NaCl 200; KCl 2; MgSO4 · 7 H2O 0.2; KH2PO4 plates. The media used for the enrichment cultures were the fol- 0.5. The pH were take to 7.0 before sterilization. The amino lowings: Eimhjellen medium: Yeast extract (Difco), 5.0 g; acids were added for filtration to the sterile basal medium at MgSO4 · 7 H2O, 2.0 g; CaCl2 · 2 H2O, 0.5 g; NaCl, 25 g; dis- 0.1% final concentration. tilled water, 100 ml (EIMHJELLEN, 1965); Sehgal and Gibbons The susceptibility to antimicrobial agents was tested on medium: Yeast extract (Difco), 1.0 g; Casamino acids (Difco), media HE 25% (w/v)total salts with antibiotic disks (Difco), by 0.75 g; Na citrate, 0.3 g; MgSO4 · 7 H2O, 2.0 g; KCl, 0.2 g; the method of Bauer et al. (1966). The antibiotic tested were: FeCl2, 0.0023 g; NaCl, 25 g; distilled water, 100 ml (SEHGAL penicillin G (10 units), kanamycin (30 mg), tetracycline (30 mg), AND GIBBONS, 1960); MH medium: Proteose-peptone nº 3 erythromycin (15 mg), streptomycin (10 mg), bacitracin (10 (Difco), 0.5 g; Yeast extract (Difco), 1.0 g; glucose, 0.1 g with units), novobiocin (30 mg), polymyxin B (300 units), ampicillin 25% (w/v) of total salts (VENTOSA et al., 1982); and the HE (10 mg), neomycin (30 mg), chloramphenicol (30 mg), gen- medium: Yeast extract (Difco), 0.5 g; glucose, 0.1 g, with 25% tamycin (10 mg) and carbenicillin (50 mg). (w/v) of total salts (TORREBLANCA et al., 1986). The MH and HE media were supplemented with penicillin (500 units/ml) The Numerical analysis stock of total salts at 30% was prepared as described SUBOV 67 differential characters were coded in binary form; positive (1931): NaCl, 23.4 g; MgCl2 · 6 H2O, 4.2 g; MgSO4 · 7 H2O, and negative results were coded as 1 and 0 respectively and non- 6.0 g; CaCl2 · 2 H2O, 0.1 g; KCl, 0.6 g; NaCO3H, 0.02 g; NaBr, comparable or missing data were coded as 9. Strain similarities 0.07 g, FeCl , 0.0005 g; distilled water, 100 ml. All the media 3 were estimated by simple matching (Ssm) (SOKAL et al., 1958), were solidified with 20 g/l Bacto-Agar (Difco) and were adjusted coefficients and clustered by the unweighted par-group method to pH 7.3 with 1 N KOH before autoclaving. The plates were of association (UPGMA) (SNEATH et al., 1973). The cophenetic incubated four weeks at 40 ºC, in sealed plastic bags and correlation was also obtained for each method. The test error checked at the end of the first and second weeks. Colonies were was estimated by examining 10 strains in duplicate (SNEATH et re-isolated by streaking on a fresh plates with the same medium. al., 1972). The computation was performed by the NT-SYS pro- Pure cultures were finally transfer to agar slants of medium with gram, using an VAX-785 computer at the Computer Center, 5 g/l of yeast extract in 25% (w/v) total salts supplemented with University of Sevilla, Sevilla, Spain. 0.1% glucose. The pH was adjusted to 7.0 with NaOH 4 M. The reference strains used in this study were the followings: Haloarcula sinaiiensis ATCC 33800, Haloarcula marismortui Electron microscopy DSM 3752, Haloarcula hispanica DSM 4426, Haloarcula cali- Transmission electron microscopy was used to exam cell forniae ATCC 33799, Haloarcula japonica DSM 6131, Haloar- morphology of representative strains from each phenon. Sam- cula vallismortis DSM 3756, Halobacterium halobium CCM ples from liquid culture were stained with 2% uranyl acetate (30 2090, Halobacterium halobium CECT 396, Halobacterium sali- sec) and then washing with 0.3% acetic acid. A TEM 902 narum CCM 2148, Halobacterium salinarum DSM 3754, (Zeiss) high resolution transmission electron microscope at 80 Halorubrum sodomense DSM 3755, Halorubrum saccharovo- Kw was used. rum DSM 1137, Halorubrum lacusprofundi DSM 5036, Halorubrum coriense DSM 10284, Halorubrum trapanicum Lipid composition CECT 397, Haloferax mediterranei ATCC 33500, Haloferax Lipid were extracted from wet cells with chloroform- gibbonsii DSM 4427 Haloferax volcanii DSM 3757, Haloferax methanol (2:1 v/v) as described by KATES (1972). The lipids were denitrificans DSM 4425 and Halococcus morrhuae NCMB 757. separated by thin-layer chromatography by single development on silica gel plates (60 F254, Merk) in chloroform-methanol- Characterization of isolates acetic acid-water (85:22:5:10:4 v/v).
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