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.
Keywordshaloalkaliphilic sulfide thiosulfate 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.
Classification and features
Genome sequencing information
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
Insights from the genome sequence
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.
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