Halophilic and Haloalkaliphilic Sulfur-Oxidizing Bacteria
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Chemotrophic sulfur-oxidizing bacteria (SOB) represent an important functional group of microorganisms responsible for the dark oxidation of reduced sulfur compounds generated by sulfidogens. Until recently, only a single genus of halophilic SOB (Halothiobacillus) has been described, and nothing was known about the ability of this group to grow at high pH.
Investigation of soda lakes, unique extremely alkaline and saline habitats, led to the discovery of a novel ecotype of natronophilic SOB. In contrast to the previously known neutrophilic ecotype, this group cannot grow at neutral pH, but grows optimally in soda brines at pH values around 10. They were the first chemolithoautotrophs among the described alkaliphiles. The group, so far, includes four novel genera within the Gammaproteobacteria. The genera Thioalkalimicrobium and Thioalkalispira represent low salt-tolerant alkaliphiles tolerating up to 1.5 M Na+. The genus Thioalkalibacter is a high salt-tolerant facultative alkaliphile. The genus Thioalkalivibrio is the most diverse and includes aerobic extremely salt-tolerant members and moderately salt-tolerant thiocyanate-utilizing and facultatively anaerobic denitrifying strains. The genome sequence of two Thioalkalivibrio strains revealed the presence of a truncated Sox system lacking the SoxCD component which is typical for gammaproteobacterial SOB. Bioenergetic studies of high salt-tolerant Thioalkalivibrio strains showed an obligate sodium dependence for respiratory activity implying the presence of sodium-dependent elements.
Investigation of hypersaline inland chloride-sulfate lakes and hypersaline brines of marine origin with neutral pH revealed an unexpectedly high culturable diversity of halophilic obligately chemolithoautotrophic SOB comprising seven different groups within the Gammaproteobacteria. Two groups of strictly aerobic moderate halophiles were represented by the known genera Halothiobacillus and Thiomicrospira. Under denitrifying conditions and with thiocyanate as e-donor, three novel groups of moderately halophilic SOB were represented by the genera Thiohalomonas, Thiohalophilus, and Thiohalobacter. At 4 M NaCl, two groups of extremely halophilic SOB (a type not known before among the SOB) had been discovered. The obligately aerobic extreme halophiles comprised a novel genus Thiohalospira, and the facultatively anaerobic nitrate-reducing extreme halophiles—a novel deep-lineage genus Thiohalorhabdus.
Overall, the investigation of hypersaline and (halo)alkaline habitats uncovered a novel and diverse world of extremophilic SOB with properties previously unknown for chemolithoautotrophic bacteria.
KeywordsSoda Lake Mono Lake Hypersaline Lake Extreme Halophile Moderate Halophile
We would like to thank our colleagues B.E. Jones, W.D. Grant, and G.A. Zavarzin for providing samples from the Kenyan soda lakes. The work was supported by grants from RFBR (recent grant 10-04-00152) and from the Dutch Science Foundations (NWO and STW).
- Banciu H, Sorokin DY, Galinski EA, Muyzer G, Kleerebezem R, Kuenen JG (2004a) Thioalkalivibrio halophilus sp. nov., a novel obligately chemolithoautotrophic facultatively alkaliphilic and extremely salt-tolerant sulfur-oxidizing bacterium from a hypersaline alkaline lake. Extremophiles 8:325–334PubMedGoogle Scholar
- Banciu H, Sorokin DY, Tourova TP, Galinski EA, Muntyan MS, Kuenen JG, Muyzer G (2008) Influence of salts and pH on growth and activity of a novel facultatively alkaliphilic, extremely salt-tolerant, obligately chemolithoautotrophic sulfur-oxidizing gammaproteobacterium Thioalkalibacter halophilus gen. nov., sp. nov. from south-western Siberian soda lakes. Extremophiles 12:391–404PubMedCrossRefGoogle Scholar
- Baumgarte S (2003) Microbial diversity of soda lake habitats. PhD thesis, Carolo-Wilhelmina University, Braunschweig, Germany, pp 79–81Google Scholar
- Eugster HP (1970) Chemistry and origins of the brines of Lake Magadi. Mineral Soc Am Spec Publ 3:215–235Google Scholar
- Gorlenko VM, Namsaraev BB, Kulyrova AV, Zavarzina DG, Zhilina TN (1999) Activity of sulfate-reducing bacteria in the sediments of the soda lakes in south-east Transbaikal area. Microbiology 68:580–586Google Scholar
- Grant WD, Tindall BJ (1986) The alkaline saline environment. In: Herbert RA, Codd GA (eds) Microbes in extreme environments. Academic, London, pp 25–54Google Scholar
- Gunde-Cimerman N, Zalar P, de Hoog S, Plemenitas A (2000) Hypersaline waters in salterns as natural ecological niches for halophilic black yeasts. FEMS Microbiol Ecol 32:235–240Google Scholar
- Horikoshi K (1991) Microorganisms in alkaline environments. Kodansha, TokyoGoogle Scholar
- Isachenko BL (1951) Chloride, sulfate and soda lakes of Kulunda steppe and its biogenic processes [in Russian]. In: Selected works, vol 2. Academy of Sciences USSR, Leningrad, pp 143–162Google Scholar
- Mori K, Suzuki K, Urabe T, Sugihara M, Tanaka K, Hamada M, Hanada S (2011) Thioprofundum hispidum sp. nov., an obligately chemolithoautotrophic sulfur-oxidizing bacterium of class Gammaproteobacteria isolated from the hydrothermal field in Suiyo Seamount, and proposal of Thioalkalispiraceae fam nov. in the order of Chromatiales. Int J Syst Evol Microbiol 61:2412–2418PubMedCrossRefGoogle Scholar
- Sorokin DY, Lysenko AM, Mityushina LL, Tourova TP, Jones BE, Rainey FA, Robertson LA, Kuenen JG (2001a) Thioalkalimicrobium aerophilum gen. nov., sp. nov. and Thioalkalimicrobium sibericum sp. nov., and Thioalkalivibrio versutus gen. nov., sp. nov., Thioalkalivibrio nitratis sp. nov. and Thioalkalivibrio denitrificans sp. nov., novel obligately alkaliphilic and obligately chemolithoautotrophic sulfur-oxidizing bacteria from soda lakes. Int J Syst Evol Microbiol 51:565–580PubMedGoogle Scholar
- Sorokin DY, Gorlenko VM, Tourova TP, Kolganova TV, Tsapin AI, Nealson KH, Kuenen JG (2002a) Thioalkalimicrobium cyclicum sp. nov. and Thioalkalivibrio jannaschii sp. nov., new species of alkaliphilic, obligately chemolithoautotrophic sulfur-oxidizing bacteria from a hypersaline alkaline Mono Lake (California). Int J Syst Evol Microbiol 52:913–920PubMedCrossRefGoogle Scholar
- Sorokin DY, Tourova TP, Lysenko AM, Mityushina LL, Kuenen JG (2002b) Thioalkalivibrio thiocyanooxidans sp. nov. and Thioalkalivibrio paradoxus sp. nov., novel alkaliphilic, obligately autotrophic, sulfur-oxidizing bacteria from the soda lakes able to grow with thiocyanate. Int J Syst Evol Microbiol 52:657–664PubMedGoogle Scholar
- Sorokin DY, Tourova TP, Bracker G, Muyzer G (2007a) Thiohalomonas denitrificans gen. no. sp. nov., and Thiohalomonas nitratireducens sp. nov., novel obligately chemolitho-autotrophic moderately halophilic thiodenitrifying Gammaproteobacteria from hypersaline habitats. Int J Syst Evol Microbiol 57:1582–1589PubMedCrossRefGoogle Scholar
- Sorokin DY, Tourova TP, Bezsoudnova EY, Pol A, Muyzer G (2007b) Denitrification in a binary culture and thiocyanate metabolism in Thiohalophilus thiocyanatoxidans gen. nov. sp. nov. – a moderately halophilic chemolithoautotrophic sulfur-oxidizing Gammaproteobacterium from hypersaline lakes. Arch Microbiol 187:441–450PubMedCrossRefGoogle Scholar
- Sorokin DY (2008) Diversity of halophilic sulfur-oxidizing bacteria in hypersaline habitats. In: Dahl C, Friedrich CG (eds) Microbial sulfur metabolism. Proceedings of the international symposium on microbial sulfur metabolism, Münster, Germany, 29 June–02 July 2006. Springer, Berlin, pp 225–237Google Scholar
- Sorokin DY, Tourova TP, Muyzer G, Kuenen JG (2008a) Thiohalospira halophila gen. nov. sp. nov., and Thiohalospira alkaliphila sp. nov., novel obligately chemolithoautotrophic extremely halophilic sulfur-oxidizing Gammaproteobacteria from hypersaline habitats. Int J Syst Evol Microbiol 58:1685–1692PubMedCrossRefGoogle Scholar
- Sorokin DY, Tourova TP, Galinski EA, Muyzer G, Kuenen JG (2008b) Thiohalorhabdus denitrificans gen. nov. sp. nov., an extremely halophilic obligately chemolithoautotrophic and facultatively anaerobic sulfur-oxidizing deep-lineage gammaproteobacterium from hypersaline habitats. Int J Syst Evol Microbiol 58:2890–2897PubMedCrossRefGoogle Scholar
- Sorokin DY, Kuenen JG, Muyzer G (2011) The microbial sulfur cycle in soda lakes. Front Microbial 2:44Google Scholar
- Tikhonova T, Slutsky A, Antipov AN, Boyko KM, Polyakov KM, Sorokin DY, Zvyagilskaya RA, Popov VO (2006) Molecular and catalytic properties of a novel cytochrome c nitrite reductase from nitrate-reducing haloalkaliphilic sulfur-oxidizing bacterium Thioalkalivibrio nitratireducens. BBA Proteins Proteom 1764:715–723CrossRefGoogle Scholar
- Tindall BJ (1988) Procaryotic life in the alkaline, saline, athalassic environment. In: Rodriguez-Valera F (ed) Halophilic bacteria. CRC Press, Boca Raton, pp 31–67Google Scholar
- Tourova TP, Spiridonova EM, Berg IA, Kuznetsov BB, Sorokin DY (2006) Occurrence, phylogeny and evolution of ribulose-1,5-bisphosphate carboxylase/oxygenase genes in obligately chemolithoautotrophic sulfur-oxidizing bacteria of the genera Thiomicrospira and Thioalkalimicrobium. Microbiology 152:2159–2169PubMedCrossRefGoogle Scholar
- Van der Wielen PWJJ, Bolhuis H, Borin S, Daffonchio D, Corselli C, Giuliano L, D’Auria G, de Lange GJ, Huebner A, Varnavas SV, Thomson J, Tamburini C, Marty D, McGenity TJ, Timmis KN (2005) The enigma of prokaryotic life in deep hypersaline anoxic basins. Science 307:121–123PubMedCrossRefGoogle Scholar
- Zavarzin GA (ed) (2007) Alkaliphilic microbial communities, vol XIV, Trans Winogradsky Inst Microbiol. Nauka, Moscow (in Russian)Google Scholar
- Zavarzin GA, Zhilina TN, Kevbrin VV (1999) The alkaliphilic microbial community and its functional diversity. Microbiology 68:503–521 (Moscow, English Translation)Google Scholar
- Zhilina TN, Zavarzin GA, Rainey FA, Pikuta EF, Osipov GA, Kostrikina NA (1997) Desulfonatronovibrio hydrogenovorans gen. nov., sp. nov., an alkaliphilic sulfate reducing bacterium. Int J Syst Evol Microbiol 47:144–149Google Scholar