- Open Access
Complete genome sequence of “Thioalkalivibrio sulfidophilus” HL-EbGr7
© The Author(s) 2011
- Published: 4 March 2011
“Thioalkalivibrio sulfidophilus” HL-EbGr7 is an obligately chemolithoautotrophic, haloalkaliphilic sulfur-oxidizing bacterium (SOB) belonging to the Gammaproteobacteria. The strain was found to predominate a full-scale bioreactor, removing sulfide from biogas. Here we report the complete genome sequence of strain HL-EbGr7 and its annotation. The genome was sequenced within the Joint Genome Institute Community Sequencing Program, because of its relevance to the sustainable removal of sulfide from bio- and industrial waste gases.
- sulfur-oxidizing bacteria (SOB)
Features of “Thioalkalivibrio sulfidophilus” strain HL-EbGR7 according to the MIGS recommendations .
Species “Thioalkalivibrio sulfidophilus” HL-EbGR7
0.2-1.5M Na+ (opt.0.4 M)
Sulfide/polysulfide, thiosulfate, sulfur
Alkaline bioreactors; soda lakes
Eerbeek, The Netherlands
Sample collection time
Apart from their role in the sulfur cycle of soda lakes, Thioalkalivibrio species also play a key role in the sustainable removal of sulfide from wastewater and gas streams. In this so-called ‘Thiopaq-process’, hydrogen sulfide is stripped from the gas phase into an alkaline solution, which is subsequently transferred to a bioreactor where Thioalkalivibrio oxidizes HS- almost exclusively to elemental sulfur at a low red-ox potential . Removal of toxic sulfide is needed, not only for a clean and healthy environment, but also to protect gas turbines from corrosion. In contrast to chemical desulfurization processes, such as the ‘Claus-process’, biological removal is cheaper, cleaner and more sustainable, as the produced hydrophilic bio-sulfur is a better fertilizer and fungicide than the chemically produced crystalline hydrophobic sulfur.
To get insight into the molecular mechanism by which Thioalkalivibrio strains adapt to haloalkaline conditions (i.e., pH 10 and up to 4 M of Na+) identification of the genes that are involved in these adaptations is needed. The most important issues are sulfide specialization, carbon assimilation at high pH and bioenergetic adaptation to high salt/high pH. In addition, information on the genome might help in optimizing the sulfur removal process. Here we present a summary classification and a set of features for “T. sulfidophilus” HL-EbGr7, together with the description of the genomic sequencing and annotation.
Genome project history
Genome sequencing project information
6kb Sanger and 454 standard libraries
ABI-3730, 454 GS FLX Titanium
8.19 × Sanger, 23.3 × pyrosequence
Less than one error per 50kb
Gene calling method
GenBank date of release
December 29, 2008
NCBI project ID
IMG Taxon ID
Source material identifier
Personal culture collection, Winogradsky Institute of Microbiology, Moscow
Growth conditions and DNA isolation
After a long-term gradual adaptation on mixed substrate medium, the isolate was able to grow solely with thiosulfate at micro-oxic conditions. The medium contained 40 mM thiosulfate as an energy source and a standard sodium carbonate-bicarbonate buffer  (Sorokin et al., 2006) at pH 10 and 0.6 M Na+. The cells were harvested by centrifugation and stored at -80°C for DNA extraction. Genomic DNA was obtained using phenol-chloroform-isoamylalcohol (PCI) extraction. Briefly, the cell pellet was suspended in a Tris-EDTA buffer at pH 8, and lysed with a mixture of SDS and Proteinase K. The genomic DNA was extracted using PCI and precipitated with ethanol. The pellet was dried under vacuum and subsequently dissolved in water. The quality and quantity of the extracted DNA was evaluated using the DNA Mass Standard Kit provided by the JGI.
Genome sequencing and assembly
The genome of “T. sulfidophilus” HL-EbGr7 was sequenced using a combination of Sanger and 454 sequencing platforms. All general aspects of library construction and sequencing can be found at the JGI website . Pyrosequencing reads were assembled using the Newbler assembler version 1.1.02.15 (Roche). Large Newbler contigs were broken into 7,722 overlapping fragments of 1,000 bp and entered into assembly as pseudo-reads. The sequences were assigned quality scores based on Newbler consensus q-scores with modifications to account for overlap redundancy and adjust inflated q-scores. A hybrid 454/Sanger assembly was made using the Parallel Genome Assembler (PGA). Possible mis-assemblies were corrected and gaps between contigs were closed by editing in Consed, or by custom primer walks of sub-clones or PCR products. A total of 518 Sanger finishing reads were produced to close gaps, to resolve repetitive regions, and to raise the quality of the finished sequence. The error rate of the completed genome sequence is less than 1 in 100,000. Together, the combination of the Sanger and 454 sequencing platforms provided a 31.49-times coverage of the genome. The final assembly contains 32,486 Sanger reads and 390,057 pyrosequencing reads.
Genes were identified using Prodigal  as part of the Oak Ridge National Laboratory genome annotation pipeline followed by a round of manual curation using the JGI GenePRIMP pipeline . The predicted CDSs were translated and used to search the National Center for Biotechnology Information (NCBI) nonredundant database, UniProt, TIGRFam, Pfam, PRIAM, KEGG, COG, and InterPro, databases. Additional gene prediction analysis and functional annotation were performed within the Integrated Microbial Genomes Expert Review (IMG-ER) platform .
% of Total
Genome size (bp)
DNA coding region (bp)
DNA G+C content (bp)
Number of replicons
Genes in paralog clusters
Genes assigned to COGs
Genes assigned Pfam domains
Genes with signal peptides
Number of genes associated with the general COG functional categories.
Amino acid transport and metabolism
Carbohydrate transport and metabolism
Cell cycle control, cell, division, chromosome partitioning
Cell wall/membrane/envelope biogenesis
Chromatin structure and dynamics
Coenzyme transport and metabolism
Energy production and conversion
General function prediction only
Inorganic ion transport and metabolism
Intracellular trafficking, secretion, and vesicular transport
Lipid transport and metabolism
Nucleotide transport and metabolism
Posttranslational modification, protein turnover, chaperones
RNA processing and modification
Replication, recombination and repair
Secondary metabolites biosynthesis, transport and catabolism
Signal transduction mechanisms
Translation, ribosomal structure and biogenesis
Not in COGs
One of the major problems of autotrophic growth at high pH is the assimilation of inorganic carbon (Ci); carbon dioxide concentrations are very low and most inorganic carbon is present as HCO3− or even as CO32− at pH values of 10 and higher. The latter is not available to the cell, which is the main reason for growth limitation of haloalkaliphilic SOB at pH above 10.5, since their energy generation respiratory system is still active up to pH 11–11.5 . Inside the cells, where Ci assimilation occurs, the pH is around 8.5, which means that HCO3− must be taken up as a substrate at an exterior pH of 10. This demands active transport by means of a Na+/HCO3-symporter, such as StbA, which has been found in the alkaliphilic cyanobacterium Synechocystis sp. strain PCC6803 . However, genes encoding StbA have not been detected in strain HLEbGr7. Another means of growth at limited CO2 concentrations is the use of a carbon-concentrating mechanism (CCM), which has been described for other autotrophic microorganisms . Part of the CCM is the presence of carboxysomes, in which ribulose-1,5-biphosphate carboxylase/oxygenase (RuBisCO) and carbonic anhydrase, the key enzymes in CO2 fixation, are located in close proximity for an efficient carbon fixation . The genome of strain HL-EbGr7 contains the genes for the large (rbcL) and small subunit (rbcS) of RuBisCO form 1Ac, and for the synthesis of a-carboxysomes, including csoSCA (formerly know as csoS3) encoding a carboxysome shell carbonic anhydrase. The latter is necessary to convert the transported HCO3- into CO2 – the actual substrate of RuBisCO. In contrast to Thiomicrospira crunogena, the genomes of Thioalkalivibrio are lacking genes for RuBisCO form 1Aq and form II, which has been confirmed by Tourova et al. . Expression studies at different CO2 concentrations in the chemolithoautotroph Hydrogenovibrio marinus indicated the preferential expression of RuBisCO form 1Ac at low CO2 concentrations and RuBisCO form 1Aq and/or form II at higher CO2 concentrations . This result indicates that our strain is indeed adapted to low CO2 concentrations.
Although we are gaining some insight into the bioenergetics of alkaliphilic heterotrophs, such as Bacillus species , it is a complete mystery how haloalkaliphilic chemolithoautotrophic bacteria obtain enough energy for growth. To generate NADH for CO2 fixation, chemolithoautotrophic bacteria, using inorganic compounds (e.g. H2S or NH3) as electron donors, have to transport electrons against the thermodynamic gradient (‘reverse electron transport’), which is an energy-requiring process. In addition, those that are living at high salt concentrations, have to invest extra energy in the production of organic compatible solutes. And thirdly, bacteria that live at high pH have to invest additional energy to maintain their pH homeostasis.
So, to obtain enough energy for growth the haloalkaliphilic chemolithoautotrophic SOB must have a special adaptation of their bioenergetics. The most obvious solution would be the presence of primary sodium pumps, such as a sodium-driven ATP synthase, but genes for this could not be detected; instead we found all the genes for a proton-driven F0F1-type ATP synthase (i.e., subunit A, B, and C of the F0 subcomplex, and subunit alpha, beta, gamma, delta, and epsilon of the F1 subcomplex). The presence of a proton-driven ATP synthase instead of a sodium-driven ATP synthase has been found in all genomes of so far studied aerobic alkaliphilic bacteria studied thus far . However, we could detect several genes encoding different sodium-dependent pumps, such as the primary sodium pump Rnf and secondary pumps, such as the Na+/H+ antiporters NhaP and Mrp, a sodium:sulfate symporter (SulP), and the sodium-depending flagellar motor PomA/B. Apart from the genes encoding the proton-translocating NADH dehydrogenase (nuoABCDEFGHIJKLMN), we also found genes (rnfABCDGE) that are homologous to the nqr genes encoding the sodium-translocating NADH:quinone oxidoreductase (Na+-NQR ,). Na+-NQR was first discovered in the marine bacterium Vibrio alginolyticus . It is coupled to the respiratory chain, and oxidizes NADH with ubiquinone as electron acceptor. The free energy released is used to generate a sodium motive force at the FAD-quinone coupling site. The presence of both a proton- and sodium-translocating NADH:quinone oxidoreductase in one organism was described previously by Takada et al. . They showed that both pumps were very active in a psychrophilic bacterium, Vibrio sp. strain ABE-1, growing at low temperatures. It is, of course, not clear what the role of either pump is in our strain, but it is tempting to speculate that they are a special adaptation to generate enough energy for growth under these extreme conditions. Future transcriptomic and proteomic studies are necessary to validate this speculation. NhaP is a Na+/H+-antiporter (a secondary sodium pump), which plays a role in the regulation of the internal pH of the cell; it pumps sodium out of the cell and leaves protons and ensuing energy generated by the respiratory chain. Furthermore, we found all 7 genes (mnhA-G) for the multisubunit Na+/H+-antiporter Mrp, which may play a similar role as NhaP. Apart from genes encoding proton-driven flagellar motors (motA/B), we also found genes encoding sodium-driven flagellar motors (pomA/B). Phylogenetic analysis of the motA/B and pomA/B grouped them with sequences of other bacteria, such as Halorhodospira halophila and Alkalilimnicola ehrlichii (results are not shown).
Thioalkalivibrio species are characterized by their tolerance to high salt concentrations, which can be up to 4.3M total sodium [2–17]. To withstand these hypersaline conditions, these species synthesize glycine-betaine as the main compatible solute. In one of the high-salt Thioalkalivibrio strains, Banciu et al.  showed a positive correlation between salinity and the intracellular glycine-betaine concentration, and found that glycine-betaine constituted 9% of cell dry weight at 4M of sodium in the culture medium. In most cases, betaine is synthesized from choline by a two-step oxidation pathway . However, an alternative route is the synthesis of betaine by a series of methylation reactions . The genome of strain HL-EbGr7 contains genes coding for glycine sarcosine N-methyltransferase and sarcosine dimethylglycine methyltransferase, that are catalyzing betaine synthesis from glycine in a three-step methylation process, i.e., glycine -> sarcosine -> dimethylglycine -> betaine. The sequences of the 2 enzymes have high similarities to sequences found in the close relatives Halorhodospira halophila and Nitrococcus mobilis. Apart from glycine-betaine Thioalkalivibrio species also produce sucrose as a minor compatible solute (up to 2.5% of cell dry weight at 2M of sodium) . The genomes of strain HL-EbGr7 contain genes coding for the enzymes sucrose synthase and sucrose phosphate synthase, which both play a role in the synthesis of sucrose. In contrast to other members of the Ectothiorhodospiraceae, i.e., Alkalilimnicola ehrlichii, and Halorhodospira halodurans, no genes were found for ectoine synthesis in the genome of HL-EbGr7.
This work was performed under the auspices of the US Department of Energy Office of Science, Biological and Environmental Research Program, and by the University of California, Lawrence Berkeley National Laboratory under contract No. DE-AC02-05CH11231, Lawrence Livermore National Laboratory under Contract No. DE-AC52-07NA27344, and Los Alamos National Laboratory under contract No. DE-AC02-06NA25396, UT-Battelle and Oak Ridge National Laboratory under contract DE-AC05-00OR22725. DS was supported financially by RFBR grant 10-04-00152.
- Sorokin DY, Kuenen JG. Haloalkaliphilic sulfur-oxidizing bacteria from soda lakes. FEMS Microbiol Rev 2005; 29:685–702. PubMed doi:10.1016/j.femsre.2004.10.005View ArticlePubMedGoogle Scholar
- Sorokin DY, Banciu H, Robertson LA, Kuenen JG. Haloalkaliphilic sulfur-oxidizing bacteria. In: The Prokaryotes. Volume 2: Ecophysiology and Biochemistry 2006; pp. 969–984. Dworkin, M., Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E. (Ed’s). Springer, New York.View ArticleGoogle Scholar
- Sorokin DY, van den Bosch PLF, Abbas B, Janssen AJH, Muyzer G. Microbiological analysis of the population of extremely haloalkaliphilic sulfur-oxidizing bacteria dominating in lab-scale sulfide-removing bioreactors. Appl Microbiol Biotechnol 2008; 80:965–975. PubMed doi:10.1007/s00253-008-1598-8View ArticlePubMedGoogle Scholar
- Field D, Garrity G, Gray T, Morrison N, Selengut J, Sterk P, Tatusova T, Thomson N, Allen MJ, Angiuoli SV, et al. The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol 2008; 26:541–547. PubMed doi:10.1038/nbt1360PubMed CentralView ArticlePubMedGoogle Scholar
- Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 1990; 87:4576–4579. PubMed doi:10.1073/pnas.87.12.4576PubMed CentralView ArticlePubMedGoogle Scholar
- Garrity GM, Holt JG. The Road Map to the Manual. In: Garrity GM, Boone DR, Castenholz RW (eds), Bergey’s Manual of Systematic Bacteriology, Second Edition, Volume 1, Springer, New York, 2001, p. 119–169.View ArticleGoogle Scholar
- List Editor. Validation of publication of new names and new combinations previously effectively published outside the IJSEM. List no. 106. Int J Syst Evol Microbiol 2005; 55: 2235–2238. doi:10.1099/ijs.0.64108-0Google Scholar
- Garrity GM, Bell JA, Lilburn T. Class III. Gamma-proteobacteria class. nov. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT (eds), Bergey’s Manual of Systematic Bacteriology, Second Edition, Volume 2, Part B, Springer, New York, 2005, p. 1.View ArticleGoogle Scholar
- Imhoff J. Order I. Chromatiales ord. nov. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT (eds), Bergey’s Manual of Systematic Bacteriology, Second Edition, Volume 2, Part B, Springer, New York, 2005, p. 1–3.View ArticleGoogle Scholar
- Imhoff JF. Reassignment of the genus Ectothiorhodospira Pelsh 1936 to a new family, Ectothiorhodospiraceae fam. nov., and emended description of the Chromatiaceae Bavendamm 1924. Int J Syst Bacteriol 1984; 34:338–339. doi:10.1099/00207713-34-3-338View ArticleGoogle Scholar
- Sorokin DY, Lysenko AM, Mityushina LL, Tourova TP, Jones BE, Rainey FA, Robertson LA, Kuenen GJ. Thioalkalimicrobium aerophilum gen. nov., sp. nov. and Thioalkalimicrobium sibericum sp. nov., and Thioalkalivibrio versutus gen. nov., sp. nov., Thioalkalivibrio nitratis sp.nov., novel and Thioalkalivibrio denitrificancs sp. nov., novel obligately alkaliphilic and obligately chemolithoau-totrophic sulfur-oxidizing bacteria from soda lakes. Int J Syst Evol Microbiol 2001; 51:565–580. PubMedView ArticlePubMedGoogle Scholar
- Banciu H, Sorokin DY, Galinski EA, Muyzer G, Kleerebezem R, Kuenen JG. Thioalkalivibrio halophilus sp. nov., a novel obligately chemolithoautotrophic, facultatively alkaliphilic, and extremely salt-tolerant, sulfur-oxidizing bacterium from a hypersaline alkaline lake. Extremophiles 2004; 8:325–334. PubMed doi:10.1007/s00792-004-0391-6PubMedGoogle Scholar
- List Editor. Notification that new names and new combinations have appeared in volume 51, part 2, of the IJSEM. Int J Syst Evol Microbiol 2001; 51:795–796. PubMedGoogle Scholar
- Classification of Bacteria and Archaea in risk groups. http://www.baua.de TRBA 466.
- Foti M, Ma S, Sorokin DY, Rademaker JLW, Kuenen GJ, Muyzer G. Genetic diversity and biogeography of haloalkaliphilic sulfur-oxidizing bacteria beloning to the genus Thioalkalivibrio. FEMS Microbiol Ecol 2006; 56:95–101. PubMed doi:10.1111/j.1574-6941.2006.00068.xView ArticlePubMedGoogle Scholar
- Sorokin DY, Kuenen JG, Jetten M. Denitrification at extremely alkaline conditions in obligately autotrophic alkaliphilic sulfur-oxidizing bacterium “Thioalkalivibrio denitrificans”. Arch Microbiol 2001; 175:94–101. PubMed doi:10.1007/s002030000210View ArticlePubMedGoogle Scholar
- Sorokin DY, Antipov AN, Kuenen JG. Complete denitrification in a coculture of haloalkaliphilic sulfur-oxidizing bacteria from a soda lake. Arch Microbiol 2003; 180:127–133. PubMed doi:10.1007/s00203-003-0567-yView ArticlePubMedGoogle Scholar
- Sorokin DY, Tourova TP, Lysenko AM, Kuenen JG. Microbial thiocyanate utilization under high alkaline conditions. Appl Environ Microbiol 2001; 67:528–538. PubMed doi:10.1128/AEM.67.2.528-538.2001PubMed CentralView ArticlePubMedGoogle Scholar
- Sorokin DY, Tourova TP, Antipov AN, Muyzer G, Kuenen JG. Anaerobic growth of the haloalkaliphilic denitrifying sulfur-oxidizing bacterium Thialkalivibrio thiocyanodenitrificans sp. nov. with thiocyanate. Microbiology 2004; 150:24352442. PubMed doi:10.1099/mic.0.27015-0View ArticleGoogle Scholar
- Janssen AJH, Lens PNL, Stams AJM, Plugge CM, Sorokin DY, Muyzer G, Dijkmane H, Van Zessene E, Luimesf P, Buisman CJN. Application of bacteria involved in the biological sulfur cycle for paper mill effluent purification. Sci Total Environ 2009; 407:1333–1343. PubMedView ArticlePubMedGoogle Scholar
- Nelson DC, Jannasch HW. Chemoautotrophic growth of a marine Beggiatoa in sulfide-gradient cultures. Arch Microbiol 1983; 136:262–269. doi:10.1007/BF00425214View ArticleGoogle Scholar
- Pruesse E, Quast C, Knittel K, Fuchs B, Ludwig W, Peplies J, Glöckner FO. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 2007; 35:7188–7196. PubMed doi:10.1093/nar/gkm864PubMed CentralView ArticlePubMedGoogle Scholar
- Ludwig W, Strunk O, Westram R, Richter L, Meier H, Kumar Y, Buchner A, Lai T, Steppi S, Jobb G. ARB: a software environment for sequence data. Nucleic Acids Res 2004; 32:1363–1371. PubMed doi:10.1093/nar/gkh293PubMed CentralView ArticlePubMedGoogle Scholar
- Liolios K, Chen IM, Mavromatis K, Tavernarakis N, Hugenholtz P, Markowitz VM, Kyrpides NC. The Genomes OnLine Database (GOLD) in 2009: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res 2010; 38:D346–D354. PubMed doi:10.1093/nar/gkp848PubMed CentralView ArticlePubMedGoogle Scholar
- DOE Joint Genome Institute. http://www.jgi.doe.gov
- Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010; 11:119. PubMed doi:10.1186/1471-2105-11-119PubMed CentralView ArticlePubMedGoogle Scholar
- Pati A, Ivanova NN, Mikhailova N, Ovchinnikova G, Hooper SD, Lykidis A, Kyrpides NC. GenePRIMP: a gene prediction improvement pipeline for prokaryotic genomes. Nat Methods 2010; 7:455–457. PubMed doi:10.1038/nmeth.1457View ArticlePubMedGoogle Scholar
- Markowitz VM, Szeto E, Palaniappan K, Grechkin Y, Chu K, Chen IM, Dubchak I, Anderson I, Lykidis A, Mavromatis K, et al. The integrated microbial genomes (IMG) system in 2007: data content and analysis tools extensions. Nucleic Acids Res 2008; 36:D528–D533. PubMed doi:10.1093/nar/gkm846PubMed CentralView ArticlePubMedGoogle Scholar
- Shibata M, Katoh H, Sonoda M, Ohkawat H, Shimoyama M, Fukuzawa H, Kaplan A, Ogawa T. Genes essential to sodium-dependent bicarbonate transport in cyanobacteria: function and phylogenetic analysis. J Biol Chem 2002; 277:18658–18664. PubMed doi:10.1074/jbc.M112468200View ArticlePubMedGoogle Scholar
- Dobrinski KP, Longo DL, Scott KM. The carbon-concentrating mechanism of the hydrothermal vent chemolithoautotroph Thiomicrospira crunogena. J Bacteriol 2005; 187:5761–5766. PubMed doi:10.1128/IB.187.16.5761-5766.2005PubMed CentralView ArticlePubMedGoogle Scholar
- Yeates TO, Kerfeld CA, Heinhorst S, Cannon GC, Shively JM. Protein-based organelles in bacteria: carboxysomes and related microcompartments. Nat Rev Microbiol 2008; 6:681–691. PubMed doi:10.1038/nrmicro1913View ArticlePubMedGoogle Scholar
- Tourova TP, Spiridonova EM, Berg IA, Slobodova NV, Boulygina ES, Sorokin DY. Phylogeny and evolution of the family Ectothiorhodospiraceae based on comparison of 16S rRNA, cbbL and nifH genes. Int J Syst Evol Microbiol 2007; 57:2387–2398. PubMed doi:10.1099/ijs.0.65041-0View ArticlePubMedGoogle Scholar
- Yoshizawa Y, Toyoda K, Arai H, Ishii M, Igarashi Y. CO2-responsive expression and gene organization of three ribulose-1,5-biphosphate carboxylase/oxygenase enzymes and carboxysomes in Hydrogenovibrio marinus strain MH-110. J Bacteriol 2004; 186:5685–5691. PubMed doi:10.1128/IB.186.17.5685-5691.2004PubMed CentralView ArticlePubMedGoogle Scholar
- Frigaard NU, Dahl C. Sulfur metabolism in photo-trophic sulfur bacteria. Adv Microb Physiol 2009; 54:103–200. PubMed doi:10.1016/S0065-2911(08)00002-7View ArticlePubMedGoogle Scholar
- Quatrini R, Appia-Ayme C, Dennis Y, Jedlicki E, Holmes DS, Bonnefoy V. Extending the models for iron and sulfur oxidation in the extreme acidophile Acidithiobacillus ferrooxidans. BMC Genomics 2009; 10: 394. PubMed doi:10.1186/1471-2164-10-394PubMed CentralView ArticlePubMedGoogle Scholar
- Kappler U. Bacterial sulfite-oxidizing enzymes. Biochim Biophys Acta 2011; 1807:1–10. PubMed doi:10.1016/j.bbabio.2010.09.004View ArticlePubMedGoogle Scholar
- Padan E, Bibi E, Ito M, Krulwich TA. Alkaline pH homeostasis in bacteria: New insights. Biochim Biophys Acta 2005; 1717:67–88. PubMed doi:10.1016/j.bbamem.2005.09.010PubMed CentralView ArticlePubMedGoogle Scholar
- Hicks DB, Liu J, Fujisawa M, Krulwich TA. F1F0-ATP synthases of alkaliphilic bacteria: Lessons from their adaptations. Biochim Biophys Acta 2010; 1797:1362–1377. PubMed doi:10.1016/j.bbabio.2010.02.028PubMed CentralView ArticlePubMedGoogle Scholar
- Verkhovsky MI, Bogachev AV. Sodium-translocating NADH:quinone oxidoreductase as a redox-driven ion pump. Biochim Biophys Acta 2010; 1797:738–746. PubMed doi:10.1016/j.bbabio.2009.12.020View ArticlePubMedGoogle Scholar
- Tokuda H, Unemoto T. A respiratory-dependent primary sodium extrusion system functioning at alkaline pH in the marine bacterium Vibrio alginolyticus. Biochem Biophys Res Commun 1981; 102:265–271. PubMed doi:10.1016/0006-291X(81)91516-3View ArticlePubMedGoogle Scholar
- Takada Y, Fukunaga N, Sasaki S. Respiration-dependent proton and sodium pumps in a psychrophilic bacterium, Vibrio sp. strain ABE-1. Plant Cell Physiol 1988; 29:207–214.Google Scholar
- Banciu H, Sorokin DY, Rijpstra WI, Sinninghe Damsté JS, Galinski EA, Takaichi S, Muyzer G, Kuenen JG. Fatty acid, compatible solute and pigment composition of the obligately chemolithoautotrophic alkaliphilic sulfur-oxidizing bacteria from soda lakes. FEMS Microbiol Lett 2005; 243:181–187. PubMed doi:10.1016/j.femsle.2004.12.004View ArticlePubMedGoogle Scholar
- Haines TH, Dencher NA. Cardiolipin: a proton trap for oxidative phosphorylation. FEBS Lett 2002; 528:35–39. PubMed doi:10.1016/S0014-5793(02)03292-1View ArticlePubMedGoogle Scholar
- Hauß T, Dantea S, Dencher NA, Haines TH. Squalene is in the midplane of the lipid bilayer: implications for its function as a proton permeability barrier. Biochim Biophys Acta 2002; 1556:149–154. PubMed doi:10.1016/S0005-2728(02)00346-8View ArticlePubMedGoogle Scholar
- Boch J, Kempf B, Schmid R, Bremer E. Synthesis of the osmoprotectant glycine betaine in Bacillus subtilis: Characterization of the gbsAB genes. J Bacteriol 1996; 178:5121–5129. PubMedPubMed CentralPubMedGoogle Scholar
- Lai MC, Yang DR, Chuang MJ. Regulatory factors associated with synthesis of the osmolyte glycine betaine in the halophilic methanoarchaeon Methanohalophilus portucalensis. Appl Environ Microbiol 1999; 65:828–833. PubMedPubMed CentralPubMedGoogle Scholar