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"Thioalkalivibrio Sulfidophilus" HL-Ebgr7 Classification and Features Has Rod-Shaped, Elongated Cells with a Polar Flagel- “T

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Standards in Genomic Sciences (2011) 4:23-35 DOI:10.4056/sigs.1483693 Complete genome sequence of “Thioalkalivibrio sulfidophilus” HL-EbGr7 Gerard Muyzer1*, Dimitry Yu Sorokin1,2, Konstantinos Mavromatis3, Alla Lapidus3, Alicia Clum3, Natalia Ivanova3, Amrita Pati3, Patrick d'Haeseleer4, Tanja Woyke3, Nikos C. Kyrpides3 1Department of Biotechnology, Delft University of Technology, Delft, The Netherlands 2Winogradsky Institute of Microbiology, Russian Academy of Sciences, Moscow, Russia 3Joint Genome Institute, Walnut Creek, California, USA 4Joint Bioenergy Institute, California, USA *Corresponding author: Gerard Muyzer Keywords: haloalkaliphilic, sulfide, thiosulfate, sulfur-oxidizing bacteria (SOB) “Thioalkalivibrio sulfidophilus” HL-EbGr7 is an obligately chemolithoautotrophic, haloalkali- philic sulfur-oxidizing bacterium (SOB) belonging to the Gammaproteobacteria. The strain was found to predominate a full-scale bioreactor, removing sulfide from biogas. Here we re- port 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. Introduction “Thioalkalivibrio sulfidophilus” HL-EbGr7 is an obli- hydrogen sulfide is stripped from the gas phase gately chemolithoautotrophic SOB using CO2 as a into an alkaline solution, which is subsequently carbon source and reduced inorganic sulfur com- transferred to a bioreactor where Thioalkalivibrio pounds as an energy source. It belongs to the genus oxidizes HS- almost exclusively to elemental sulfur Thioalkalivibrio. This genus is characterized by at a low red-ox potential [21]. Removal of toxic obligate haloalkaliphily and forms a monophyletic sulfide is needed, not only for a clean and healthy group within the family Ectothiorhodospiraceae. environment, but also to protect gas turbines from The genus currently includes nine validly described corrosion. In contrast to chemical desulfurization species [1] and many yet uncharacterized isolates processes, such as the ‘Claus-process’, biological [2,3]. The members are slow growing and well- removal is cheaper, cleaner and more sustainable, adapted to hypersaline (up to salt saturation) and as the produced hydrophilic bio-sulfur is a better alkaline (up to pH 10.5) conditions. They can oxid- fertilizer and fungicide than the chemically pro- ize sulfide, thiosulfate, elemental sulfur, sulfite and duced crystalline hydrophobic sulfur. polythionates (see Table 1 for summary). Moreo- To get insight into the molecular mechanism by ver, some species can reduce nitrate, nitrite or nitr- which Thioalkalivibrio strains adapt to haloalkaline ous oxide [17,18] or utilize thiocyanate (SCN-) as an conditions (i.e., pH 10 and up to 4 M of Na+) identifi- energy and nitrogen source [19,20]. Genetic diver- cation of the genes that are involved in these adapta- sity analysis of 85 Thioalkalivibrio strains isolated tions is needed. The most important issues are sul- from different soda lakes located in Mongolia, fide specialization, carbon assimilation at high pH Kenya, California, Egypt and south Siberia, indi- and bioenergetic adaptation to high salt/high pH. In cated a high genetic diversity and an endemic cha- addition, information on the genome might help in racter, i.e., the majority of the genotypes (85.9%) optimizing the sulfur removal process. Here we were found to be unique to one region [15]. present a summary classification and a set of fea- Apart from their role in the sulfur cycle of soda tures for “T. sulfidophilus” HL-EbGr7, together with lakes, Thioalkalivibrio species also play a key role in the description of the genomic sequencing and anno- the sustainable removal of sulfide from wastewater tation. and gas streams. In this so-called ‘Thiopaq-process’, The Genomic Standards Consortium "Thioalkalivibrio sulfidophilus" HL-EbGr7 Classification and features has rod-shaped, elongated cells with a polar flagel- “T. sulfidophilus” HL-EbGr7 was isolated from a lum (Figure 1b and c). The strain is obligately al- full-scale Thiopaq bioreactor in the Netherlands kaliphilic with a pH optimum of 9.5. It can tolerate a salinity of 1.5 M (optimum at 0.4 M) of total so- used to remove H2S from biogas [21]. The reactor biomass had a very peculiar property, which made dium, sulfide concentrations up to 5 mM and a it different from the usual SOB biomass, i.e., an temperature up to 40°C. It utilizes ammonium and almost complete sulfide specialization and no thi- urea, but not nitrate or nitrite, as a N-source. On osulfate-oxidizing activity. This was probably the the basis of 16S rRNA gene sequencing the strain result of a very low red-ox potential at which the belongs to the Gammaproteobacteria with Thioal- reactor was operated. Therefore, the dominant kalivibrio denitrificans as the closest, described SOB could originally be enriched only with sulfide species (Figure 2). Despite this relation, strain HL- as substrate in cylinders with agarose-stabilized EbGr7 cannot grow anaerobically with NOx. Both medium containing opposing gradients of oxygen phylogeny and specific physiology indicate that and sulfide [Figure 1a, 22]. Subsequently, the this strain represents a novel species within the strain was purified using serial dilutions in gra- genus Thioalkalivibrio for which a tentative spe- dient cultures and finally from a colony on solid cies epithet “sulfidophilus” is proposed. medium with sulfide at micro-oxic conditions. It Figure 1. a, Enrichment of “Thioalkalivibrio sulfidophilus” HL-EbGr7 in a gradient culture, whereby sulfide is diffusing from an agarose plug in the bottom of the cylinder and O2 from the top. The bacterial cells ac- cumulate in a dense band at the most favorable sulfide and oxygen concentration. b, phase-contrast microphotograph; c, electron micro- scopy microphotograph of a total cell preparation contrasted with phosphotungstic acid. 24 Standards in Genomic Sciences Muyzer et al. Table 1. Features of “Thioalkalivibrio sulfidophilus” strain HL-EbGR7 according to the MIGS recommendations [4]. MIGS ID Property Term Evidence code Current classification Domain Bacteria TAS [5] Phylum Proteobacteria TAS [6] Class Gammaproteobacteria TAS [7,8] Order Chromatiales TAS [7,9] Family Ectothiorhodospiraceae TAS [10] Genus Thioalkalivibrio TAS [11-13] Species “Thioalkalivibrio sulfidophilus” HL-EbGR7 NAS Gram stain negative TAS [2] Cell shape rod-shaped TAS [2] Motility motile TAS [2] Sporulation non-sporulating TAS [2] Temperature range Mesophile TAS [2] Optimum temperature 34 TAS [2] MIGS-6.3 Salinity range 0.2-1.5M Na+ (opt.0.4 M) TAS [2] MIGS-22 Oxygen requirement microaerophilic TAS [2] - Carbon source HCO3 TAS [2] Energy source Sulfide/polysulfide, thiosulfate, sulfur TAS [2] MIGS-6 Habitat Alkaline bioreactors; soda lakes TAS [2] MIGS-15 Biotic relationship free-living TAS [2] MIGS-14 Pathogenicity none NAS Biosafety level 1 TAS [14] Isolation Thiopaq bioreactor TAS [15] MIGS-4 Geographic location Eerbeek, The Netherlands TAS [15] MIGS-5 Sample collection time 2005 NAS MIGS-4.1 Latitude 52.11 TAS [16] MIGS-4.2 Longitude 6.07 TAS [16] MIGS-4.3 Depth Not applicable MIGS-4.4 Altitude Sea level NAS Evidence codes - IDA: Inferred from Direct Assay (first time in publication); TAS: Traceable Author Statement (i.e., a direct report exists in the literature); NAS: Non-traceable Author Statement (i.e., not directly observed for the living, isolated sample, but based on a generally accepted property for the species, or anecdotal evidence). These evidence codes are from of the Gene Ontology project. If the evidence code is IDA, then the property was directly observed by one of the authors or an expert mentioned in the acknowledgements. Genome sequencing information Genome project history Strain HL-EbGr7 was selected for sequencing in NC_011901. The genome project is listed in the the 2007 Joint Genome Institute Community Se- Genome OnLine Database (GOLD) [25] as project quencing Program, because of its relevance to Gc00934. Sequencing was carried out at the Joint bioremediation. A summary of the project infor- Genome Institute (JGI). Finishing was done by JGI- mation is presented in Table 2. The complete ge- Los Alamos National Laboratory (LANL) and ini- nome sequence was finished in December 2008. tial automatic annotation by JGI-Oak Ridge Na- The GenBank accession number for the project is tional Laboratory (ORNL). http://standardsingenomics.org 25 "Thioalkalivibrio sulfidophilus" HL-EbGr7 Figure 2. Phylogenetic tree based on 16S rRNA sequences showing the phylogenetic position of “Thioalkalivibrio sulfidophilus” HL-EbGr7. The sequence was aligned to sequences stored in the SILVA database using the SINA We- baligner [23]. Subsequently, the aligned sequences were imported into ARB [24], and a neighbor joining tree was constructed. Sequences of members from the Alphaproteobacteria were used as an outgroup, but were pruned from the tree. The scale bar indicates 1% sequence difference. Growth conditions and DNA isolation After a long-term gradual adaptation on mixed at the JGI website [26]. Pyrosequencing reads substrate medium, the isolate was able to grow were assembled using the Newbler assembler solely with thiosulfate at micro-oxic conditions. version 1.1.02.15 (Roche). Large Newbler contigs The medium contained 40 mM thiosulfate as an were broken into 7,722 overlapping fragments of energy source and a standard sodium carbonate- 1,000 bp and entered
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