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Desulfonatronovibrio Halophilus Sp. Nov., a Novel Moderately Halophilic Sulfate-Reducing Bacterium from Hypersaline Chloride–Sulfate Lakes in Central Asia

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Desulfonatronovibrio Halophilus Sp. Nov., a Novel Moderately Halophilic Sulfate-Reducing Bacterium from Hypersaline Chloride–Sulfate Lakes in Central Asia Extremophiles (2012) 16:411–417 DOI 10.1007/s00792-012-0440-5 ORIGINAL PAPER Desulfonatronovibrio halophilus sp. nov., a novel moderately halophilic sulfate-reducing bacterium from hypersaline chloride–sulfate lakes in Central Asia D. Y. Sorokin • T. P. Tourova • B. Abbas • M. V. Suhacheva • G. Muyzer Received: 10 February 2012 / Accepted: 22 March 2012 / Published online: 10 April 2012 Ó The Author(s) 2012. This article is published with open access at Springerlink.com Abstract Four strains of lithotrophic sulfate-reducing soda lakes. The isolates utilized formate, H2 and pyruvate as bacteria (SRB) have been enriched and isolated from electron donors and sulfate, sulfite and thiosulfate as electron anoxic sediments of hypersaline chloride–sulfate lakes in acceptors. In contrast to the described species of the genus the Kulunda Steppe (Altai, Russia) at 2 M NaCl and pH Desulfonatronovibrio, the salt lake isolates could only tolerate 7.5. According to the 16S rRNA gene sequence analysis, high pH (up to pH 9.4), while they grow optimally at a neutral the isolates were closely related to each other and belonged pH. They belonged to the moderate halophiles growing to the genus Desulfonatronovibrio, which, so far, included between 0.2 and 2 M NaCl with an optimum at 0.5 M. On the only obligately alkaliphilic members found exclusively in basis of their distinct phenotype and phylogeny, the described halophilic SRB are proposed to form a novel species within the genus Desulfonatronovibrio, D. halophilus (type strain T T T Communicated by A. Oren. HTR1 = DSM24312 = UNIQEM U802 ). The GenBank/EMBL accession numbers of the 16S rRNA gene Keywords Sulfate-reducing bacteria (SRB) Á sequences of the HTR strains are GQ922847, HQ157562, HQ157563 and JN408678; the dsrAB gene sequences of (halo)alkaliphilic SRB Desulfonatronovibrio Á Hypersaline lakes Á Halophilic obtained in this study are JQ519392-JQ519396. Electronic supplementary material The online version of this Introduction article (doi:10.1007/s00792-012-0440-5) contains supplementary material, which is available to authorized users. Hypersaline intra-continental (athalassohaline) salt lakes D. Y. Sorokin (&) Á T. P. Tourova represent an extreme type of habitats where halophilic Winogradsky Institute of Microbiology, Russian Academy prokaryotes are a dominant form of life (Oren 2002). The of Sciences, Prospect 60-let Octyabrya 7/2, 117811 Moscow, Russia sulfur cycle is definitely active in the sediments of these e-mail: [email protected]; [email protected] lakes, judging from the presence of diverse population of halophilic sulfur-oxidizing bacteria (Sorokin 2008) and the D. Y. Sorokin Á B. Abbas Á G. Muyzer apparent sulfidogenic activity manifested by the presence Environmental Biotechnology Group, - Department of Biotechnology, Delft University of Technology, of high concentrations of FeS/HS in the top sediment Delft, The Netherlands layer and measurable activity of sulfate reduction, albeit at salinities much lower than salt saturation (Brandt et al. M. V. Suhacheva 2001; Sørensen et al. 2004; Waldron et al. 2007). Bioengineering Centre, Russian Academy of Sciences, Prospect 60-let Octyabrya 7/1, 117811 Moscow, Russia Our recent study on sulfidogenesis in anoxic sediments of hypersaline chloride–sulfate lakes in Kulunda Steppe Present Address: (Altai, Russia) (Sorokin et al. 2012) demonstrated the G. Muyzer presence of several groups of moderately halophilic SOB Department of Aquatic Microbiology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, there, most of which were highly similar to the phylotypes Amsterdam, The Netherlands found previously in the Great Salt Lake in Utah (USA) 123 412 Extremophiles (2012) 16:411–417 Fig. 1 Cell morphology of strains HTR1 (a, c) and HTR6 (b, d) grown at pH 8 and 1 M NaCl with formate and thiosulfate. a, b phase contrast microphotographs, c, d electron microphotograph of positively stained cells (Brandt et al. 1999, 2001; Jakobsen et al. 2006; Kjeldsen located in the southern part of the Kulunda Steppe, south- et al. 2007, 2010). There was, however, one exception, i.e., western Siberia (Altai, Russia). The lake brines had a pH a group of four strains obtained directly or indirectly with range of 7.6–8.2, a salinity from 125 to 340 g l-1, a sulfate formate as electron donor. These moderately halophilic content from 0.13 to 1.4 M and an acid labile sulfides SRB, unexpectedly, were identified as members of the (FeS ? HS-) content from 0.3 to 17 mM. The individual genus Desulfonatronovibrio—a typical representative of sediments were mixed in equal proportions to make a alkaliphilic SRB found previously exclusively in soda single inoculum used to enrich for halophilic SRB. lakes (Zhilina et al. 1997; Sorokin et al. 2011). In this report, we describe the properties of a novel halophilic member within the genus Desulfonatronovibrio, Enrichment and cultivation which is proposed to form a novel species D. halophilus. Enrichment and routine cultivation of halophilic SRB was performed at 28 °C on a mineral medium containing 2 M Methods NaCl buffered with 0.1 M HEPES at pH 7.5 as described previously (Sorokin et al. 2012). The pH dependence was Samples examined at Na? content of 1 M, using the following filter- sterilized buffers: for pH 6–8, 0.1 M HEPES and NaCl/ Sediment samples of the top 10 cm layer were obtained in NaHCO3; for pH 8.5–10, a mixture of sodium bicarbonate/ July 2010 from four hypersaline chloride–sulfate lakes sodium carbonate containing 0.1 M NaCl. To study the 123 Extremophiles (2012) 16:411–417 413 a HTR10, HQ157562 0.05 100 HTR9, JN408678 100 HTR1, GQ922847 100 HTR6, HQ157563 Desulfonatronovibrio hydrogenovorans Z-7935T, X99234 T 100 83 Desulfonatronovibrio magnus AHT22 , GU196831 Desulfonatronovibrio thiodismutans AHT9 (FJ469579) Desulfohalobiaceae Desulfonatronospira thiodismutans ASO3-1T, EU296537 98 100 Desulfonatronospira delicata AHT6 T, EU296539 Desulfohalobium retbaense DSM 5692T, X99235 91 Desulfohalobiaceae bacterium HTR8, HQ157564 100 Desulfohalobium utahense EtOH3T, DQ067421 100 Desulfovermiculus halophilus 11T, DQ139408 Desulfomicrobium baculatum VKM B-1378T, AF030438 Desulfomicrobiaceae Desulfovibrio alkalitolerans RT2 T, AY649785 T Desulfovibrio tunisiensis RB22 , EF577029 Desulfovibrionaceae 100 Desulfovibrio oxyclinae PIBT, U33316 b Desulfonatronovibrio thiodismutans ASO4-5, JQ519395 Desulfonatronovibrio magnus AHT22, JQ519394 Desulfonatronovibrio halophilus HTR1, JQ519392 Desulfonatronovibrio hydrogenovorans, AF418197 Desulfonatronospira thiodismutans AHT8, JQ519392 Desulfonatronospira thiodismutans ASO3-1, EF055384 Desulfonatronum lacustre, AF418189 Desulfonatronum thioautotrophicum ASO3-6, JQ519396 Desulfohalobium retbaense, AF418190 Desulfohalobium utahense, DQ386236 Desulfomicrobium baculatum, AF482460 Desulfovibrio intestinalis, AB061539 Desulfovibrio desulfuricans, DSM642, Essex 6, AF273034 Desulfovibrio piger, AB061534 Desulfovibrio termitidis, AF418185 Desulfovibrio vulgaris, U16723 Desulfovibrio marinisediminis, AB218445 Desulfovibrio desulfuricans subsp. aestuarii, strain sylt 3, AJ289157 Desulfovibrio burkinensis, AF418186 Desulfovibrio fructosivorans, AF418187 Desulfovibrio butyratiphilus, AB490775 Desulfovibrio alkalitolerans, AY864856 Desulfovibrio africanus, AF271772 Desulfovibrio aespoeensis, AF492838 Desulfovibrio halophilus, AF482461 0.10 Fig. 2 Phylogenetic position of HTR strains within the order bold. The dsrAB gene-based tree topography and evolutionary Desulfovibrionales based on 16S rRNA gene (a) and dsrAB gene distances are obtained by the Maximum Likelihood method, RAxML (b) sequence analysis. Tree 16S rRNA gene tree topography and using 250 round of bootstrap (C90 % is indicated by a solid dot) and evolutionary distances are obtained by the neighbor-joining method species AF418190 as a filter. In total 769 positions were used for with Jukes and Cantor distances. The numbers on the nodes indicate calculation. All halophilic representatives are in bold bootstrap values above 80 %. The halophilic representatives are in 123 414 Extremophiles (2012) 16:411–417 (a) (b) 100 100 90 90 80 80 70 70 60 60 50 50 40 40 30 30 20 20 10 Activity, % of maximum 10 0 0 Sulfide production, % of maximum 6.5 7 7.5 8 8.5 9 9.5 10 10.5 6.5 7 7.5 8 8.5 9 9.5 10 10.5 11 Final pH Final pH Fig. 3 Influence of pH at 1 M NaCl on growth (a) and sulfidogenic formate/acetate ? thiosulfate and the washed cells were tested with activity of resting cells (b) of strain HTR1 from salt lakes in formate ? thiosulfate. Closed circles HTR1, open circles AHT9. The comparison with Desulfonatronovibrio thiosulfatophilum AHT9 from results represent average values obtained in from 2 duplicates soda lakes (grown at 0.6 M Na?). Both organisms were grown with influence of salt concentration on growth, the HEPES- 100 buffered media with pH 7.5 containing 0.2 and 4 M NaCl 90 were mixed in different proportions. 80 70 Analytical procedures 60 50 Sulfide was measured colorimetrically (Tru¨per and Schle- 40 gel 1964) after precipitation in 10 % (w/v) Zn acetate. Cell 30 protein was determined according to Lowry et al. (1951) 20 after removal of sulfide/thiosulfate and washing the cell 10 pellet several times with 2 M NaCl containing 0.05 M Sulfide production, % of maximum 0 HCl. Phase contrast microphotographs were obtained with 0 0.5 1 1.5 2 2.5 3 a Zeiss Axioplan Imaging 2 microscope (Go¨ttingen, Ger- Na+, M many). For electron microscopy, the cells were negatively Fig. 4 Influence of NaCl at pH 8 on growth (closed circles)
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