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Complete genome sequence of Desulfurivibrio alkaliphilus strain AHT2T, a haloalkaliphilic sulfidogen from Egyptian hypersaline alkaline lakes

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Standards in Genomic Sciences201611:67

  • Received: 16 May 2016
  • Accepted: 25 August 2016
  • Published:


Desulfurivibrio alkaliphilus strain AHT2T is a strictly anaerobic sulfidogenic haloalkaliphile isolated from a composite sediment sample of eight hypersaline alkaline lakes in the Wadi al Natrun valley in the Egyptian Libyan Desert. D. alkaliphilus AHT2T is Gram-negative and belongs to the family Desulfobulbaceae within the Deltaproteobacteria. Here we report its genome sequence, which contains a 3.10 Mbp chromosome. D. alkaliphilus AHT2T is adapted to survive under highly alkaline and moderately saline conditions and therefore, is relevant to the biotechnology industry and life under extreme conditions. For these reasons, D. alkaliphilus AHT2T was sequenced by the DOE Joint Genome Institute as part of the Community Science Program.


  • Deltaproteobacteria
  • Soda lake
  • Sediment
  • Sulfur cycle
  • Sulfur disproportionation


Soda lakes are extreme environments with high salinity and highly alkaline pH values. They are formed in arid regions where high rates of evaporation lead to the accumulation of sodium carbonate salts, which are dominant in these distinctive lakes. Soda lakes support an active microbial sulfur cycle, enhanced by the stability of intermediate sulfur species such as thiosulfate and polysulfides and much lower toxicity of sulfide at these elevated pH conditions. Correspondingly, a wide variety of anaerobic haloalkaliphiles active in the reductive sulfur cycle have been isolated from these lakes [1]. Insights into sulfur redox processes will contribute to understanding how haloalkaliphilic organisms survive and thrive under dual extreme conditions. Some metabolic processes within the reductive sulfur cycle are more favorable under alkaline pH conditions than under circumneutral conditions, such as the disproportionation of elemental sulfur [2]. These sulfur redox processes are not only relevant in natural haloalkaline environments, some wastewater and gas desulfurization treatment plants are often operated at high salt concentrations and pH values where haloalkaliphiles play a role in the remediation of the affected areas. Thus, the haloalkaliphile Desulfurivibrio alkaliphilus strain AHT2T was sequenced for its relevance to sulfur cycling and the environmental biotechnology sector by the DOE-JGI Community Science Program.

Organism information

Classification and features

D. alkaliphilus AHT2T is the type strain of the Desulfurivibrio alkaliphilus species and was isolated from a mixed sediment sample from eight hypersaline alkaline lakes in the Wadi al Natrun valley in the Libyan Desert (Egypt) [3]. The cells are Gram-negative, non-motile, curved rods that do not form spores (Fig. 1). D. alkaliphilus AHT2T tolerates sodium carbonate concentrations ranging from 0.2 - 2.5 M total Na+ and grows within a pH range of 8.5 - 10.3 (optimum at pH 9.5) [3]. Phylogenetic analysis showed that the strain belongs to the family Desulfobulbaceae within the Deltaproteobacteria and is most closely related to a, so far undescribed, haloalkaliphilic chemoautotrophic sulfur-disproportionator within the same genus: Desulfurivibrio sp. strain AMeS2 [2]. Strains AMeS2 and AHT2T are, so far, the only known representatives of the Desulfurivibrio genus (Fig. 2). The closest sequenced relative to this novel genus, is another soda lake isolate delta proteobacterium sp. MLMS-1, which has been enriched as an arsenate-dependent sulfide oxidizer [4]. D. alkaliphilus AHT2T is able to reduce thiosulfate and elemental sulfur [3] and plays a role in the reductive sulfur cycle in soda lake environments [1]. D. alkaliphilus AHT2T is also capable of chemolithoautotrophic growth through the disproportionation of elemental sulfur under alkaline pH conditions without iron(III) oxides [2], which are normally required by neutrophilic sulfur disproportionators. More classifications and features are listed in Table 1.
Fig. 1
Fig. 1

Morphology of D. alkaliphilus AHT2T. a A phase contrast micrograph of the D. alkaliphilus AHT2T cells. b A scanning electron microscope image of the D. alkaliphilus AHT2T cells

Fig. 2
Fig. 2

Neighbour joining tree based on 16S rRNA gene sequences showing the phylogenetic position of D. alkaliphilus AHT2T to other species within the Deltaproteobacteria class. The Firmicutes were used as an outgroup and subsequently pruned from the tree. The black dots indicate a bootstrap value between 80 and 100 %. The scale bar indicates a 1 % sequence difference. The tree was constructed with the ARB software package [37] and the SILVA database [19]. The bootstrap values were calculated using MEGA-6 [38]

Table 1

Classification and general features of D. alkaliphilus AHT2T




Evidence code



Domain: Bacteria

TAS [39]

Phylum: Proteobacteria

TAS [40, 41]

Class: Deltaproteobacteria

TAS [42, 43]

Order: Desulfobacterales

TAS [43, 44]

Family: Desulfobulbaceae

TAS [43, 45]

Genus: Desulfurivibrio

TAS [3, 46]

Species: Desulfurivibrio alkaliphilus

TAS [3, 46]

Type strain: AHT2T

TAS [3]


Gram stain



Cell shape






Temperature range


Optimum temperature



pH range; Optimum

8.5–10.3; 9.5

TAS [3]

Carbon source

acetate, HCO3

TAS [3]



hypersaline alkaline lake sediments




moderately salt-tolerant


Oxygen requirement



Biotic relationship

free living





Geographic location

Wadi al Natrun, Libyan Desert (Egypt)


Sample collection

September 2000


Latitude – Longitude

30° 24′ N



30° 18′ E




0–10 cm

TAS [3]



−20 m


Genome sequencing information

Genome project history

D. alkaliphilus AHT2T was sequenced by the DOE Joint Genome Institute [5] based on its relevance to the biotechnology industry. It is part of the Community Science Program (CSP_788492) entitled ‘Haloalkaliphilic sulfate-, thiosulfate- and sulfur-reducing bacteria’. The project is registered in the Genomes Online Database (Ga0028523) [6] and the complete genome sequence is deposited in GenBank (GCA_000092205). Sequencing and assembly were performed at the DOE Joint Genome Institute using state of the art sequencing technology [7]. A summary of the project information is shown in Table 2.
Table 2

Project information





Finishing quality



Libraries used

Solexa, 454


Sequencing platforms

454, Illumina


Fold coverage

39.9 × 454, 98 × Illumina



Newbler,Velvet, phrap


Gene calling method

Prodigal [17]


Locus Tag


Genbank ID


Genbank Date of Release







Project relevance


Growth conditions and genomic DNA preparation

D. alkaliphilus AHT2T was grown anaerobically at 30 °C in Na-carbonate buffered mineral medium containing 0.6 M total Na+ with a pH of 10. 4 mM NH4Cl, 1 mM MgCl2 x 6H2O, 1 ml L−1 trace element solution [8], 2 mM Na-acetate as C-source and ~5 g/L powdered sulfur (electron acceptor) were added after sterilization. 2 L culture was grown in a 10 L bottle mounted on a magnetic stirrer with an 0.5 bar H2 (electron donor) overpressure head-space. The cells from 1 L culture were harvested by centrifugation at 13,000 g for 30 min, washed with 1 M NaCl and stored at −80 °C. The DNA was extracted and purified from frozen pellets by the phenol-chloroform method after pre-treatment with SDS-proteinase K according to Murmur [9]. The purity and molecular weight of the DNA was checked by UV spectroscopy and gel electrophoresis, respectively.

Genome sequencing and assembly

The total size of the D. alkaliphilus AHT2T genome sequence assembly was 3.1 Mbp. The draft genome of D. alkaliphilus AHT2T was generated at the DOE Joint Genome Institute using a combination of Illumina [10] and 454 DNA sequencing technologies [11]. An Illumina GAii shotgun library was constructed, which generated 3,998,684 reads and a 454 Titanium standard library, which generated 517,041 reads totalling 123.6 Mb of 454 data. The initial draft assembly contained 57 contigs in 1 scaffold. The 454 Titanium data were assembled with Newbler, The Newbler consensus sequences were computationally shredded into 2 kb overlapping fake reads (shreds). Illumina sequencing data was assembled with VELVET, version 1.0.13 [12], and the consensus sequences were computationally shredded into 1.5 kb overlapping fake reads (shreds). We integrated the 454 Newbler consensus shreds and the Illumina VELVET consensus shreds using parallel Phrap, version SPS - 4.24 (High Performance Software, LLC). The software Consed [13] was used in the finishing process as described previously [14]. The final assembly is based on 123.6 Mb of 454 draft data which provides an average 39.9x coverage of the genome and 303.9 Mb of Illumina draft data providing an average 98x coverage of the genome.

Genome annotation

The complete genome sequence was annotated using the JGI Prokaryotic Automatic Annotation Pipeline [15] with additional manual review using the Integrated Microbial Genomes - Expert Review platform [16]. Genes were predicted using Prodigal [17], followed by a round of manual curation using the JGI GenePRIMP pipeline [18]. Ribosomal RNAs were detected using models built from SILVA [19] and tRNAs were predicted with tRNAScanSE [20]. The predicted coding sequences were translated and used to search the National Center for Biotechnology Information non-redundant database, UniProt, TIGRFam, Pfam, KEGG, COG and InterPro databases. Further annotation was performed using the Integrated Microbial Genomes platform. The final annotated genome is available from the Integrated Microbial Genome system [21].

Genome properties

The genome is 3,097,763 bp long with GC content of 60.29 % (Table 3). 2732 genes were found, of which 2676 are annotated as protein-coding genes and 56 are RNA genes (47 tRNA genes). A total of 75 % of the protein-coding genes have been assigned a function prediction and 62.26 % have been assigned to a COG (Table 3). The number of genes assigned to each functional COG category is listed in Table 4.
Table 3

Nucleotide content and gene count levels of the genome



% of total

Genome size (bp)



DNA coding (bp)



DNA G + C (bp)



DNA scaffolds



Total genes



Protein coding genes



RNA genes



Pseudo genes



Genes in internal clusters



Genes with function prediction



Genes assigned to COGs



Genes with Pfam domains



Genes with signal peptides



Genes with transmembrane helices



CRISPR repeats


Table 4

Number of genes associated with general COG functional categories



% of total





Translation, ribosomal structure and biogenesis




RNA processing and modification








Replication, recombination and repair




Chromatin structure and dynamics




Cell cycle control, cell division, chromosome partitioning




Defense mechanisms




Signal transduction mechanisms




Cell wall/membrane biogenesis




Cell motility




Intracellular trafficking and secretion




Posttranslational modification, protein turnover, chaperones




Energy production and conversion




Carbohydrate transport and metabolism




Amino acid transport and metabolism




Nucleotide transport and metabolism




Coenzyme transport and metabolism




Lipid transport and metabolism




Inorganic ion transport and metabolism




Secondary metabolites biosynthesis, transport and catabolism




General function prediction only




Function unknown




Not in COGs

Extended insights from the genome sequence

Carbon fixation

In order to grow chemolithoautotrophically, D. alkaliphilus AHT2T assimilates inorganic carbon from the environment. The genome of D. alkaliphilus AHT2T contains the key genes necessary for the WL pathway, a mode of carbon fixation from CO2, which can run in the reductive and oxidative direction [22]. In the reductive direction, carbon is fixed from inorganic CO2 to cell material. The WL pathway functions in this direction in many representatives of sulfate-reducing bacteria within the Deltaproteobacteria . Some organisms may couple the reverse, or oxidative, direction to sulfate reduction. The WL gene clusters have previously been defined for delta proteobacterium sp. MLMS-1 from Mono Lake [23], the closest sequenced relative of D. alkaliphilus AHT2T (Fig. 2). Here we identified the WL genes necessary for carbon fixation by comparing the corresponding delta proteobacterium sp. MLMS-1 gene clusters to those present in D. alkaliphilus AHT2T using the JGI IMG database (Fig. 3). The first step in the reductive pathway is the reduction of CO2 to formate, by formate dehydrogenase (DaAHT2_0823 and an accessory protein DaAHT2_0820). This is followed by formyl-THF synthetase (DaAHT2_0837) and a methylene-THF dehydrogenase/cyclohydrolase (DaAHT2_0828) and a methylene-THF reductase (DaAHT2_0827). The acs gene cluster is necessary for the carbonyl branch of the reaction [22], which starts with the reduction of CO2 to carbon monoxide by a carbon monoxide dehydrogenase (DaAHT2_0826). In the last step, the products of the carbonyl and methyl branch are combined to form the product acetyl-CoA, by a CO dehydrogenase/acetyl-CoA synthase complex (DaAHT2_0825 and DaAHT2_0824). The end product of the WL cycle is typically acetate, however, the genes needed to convert acetyl-CoA to the end product acetate are absent in the D. alkaliphilus AHT2T genome, resulting in acetyl CoA being the carbon end product which can be incorporated into biomass.
Fig. 3
Fig. 3

D. alkaliphilus AHT2T Wood-Ljungdahl pathway genes, including the acs gene cluster, based on delta proteobacterium sp. MLMS-1 [23]. The gene locus tags are depicted beneath the illustrated gene representations

Sulfur cycle

Culture studies have provided evidence that D. alkaliphilus AHT2T is able to reduce a number of different sulfur redox species to conserve energy [4]. The dsr cluster catalyzes sulfite reduction to sulfide [24, 25], which is also present in the D. alkaliphilus AHT2T genome consisting of dsrABC (DaAHT2_0296, DaAHT2_0297, DaAHT2_2041) and dsrMK(JOP) (DaAHT2_2298-DaAHT2_2302). D. alkaliphilus AHT2T also has genes which may be involved in the oxidative branch of sulfite disproportionation: a sulfate adenylyltransferase sat (DaAHT2_0293) and two adenylylsulfate reductase subunits aprAB (alpha: DaAHT2_1471 and beta: DaAHT2_1472). In the haloalkaline environment from which D. alkaliphilus AHT2T was isolated, intermediate redox species of sulfur such as polysulfides and thiosulfate are abundantly present. The genes for the reduction of elemental sulfur (polysulfides) and thiosulfate (psr/phs) are annotated together as a single KEGG ortholog, namely K08352 [26]. However, the psr and phs genes have been identified individually in different organisms and are responsible for different reactions.

The molybdenum-containing polysulfide reductase gene psrA (WS0116 / Ga0076602_11110) was first identified in the sulfur/polysulfide-reducing epsilonproteobacterium Wolinella succinogenes [27, 28]. The thiosulfate reductase operon phs (STY2271-STY2269) was first identified in the enteric bacterium Salmonella typhimurium [29, 30]. The genome of D. alkaliphilus AHT2T contains two molybdopterin oxidoreductases (DaAHT2_0547 and DaAHT2_0420) (Fig. 4a). In order to determine whether the D. alkaliphilus AHT2T gene cluster is a psr or a phs operon, we used eggNOG 4.5 [31] to find 446 orthologs of psrA (WS0116 / Ga0076602_11110) in 233 species, from which a phylogenetic neighbor-joining tree was constructed and trimmed (Fig. 4b). The molybdopterin oxidoreductase sequences of D. alkaliphilus AHT2T (DaAHT2_0420 and DaAHT2_0547) did not cluster within the psr or phs branch (Fig. 4b). Nevertheless, they are part of the same orthologous group as the W. succinogenes psrA (ENOG4107QY8) with which they share 24,80 % (DaAHT2_0547) and 31,75 % (DaAHT2_0420) identity. The S. typhimurium phsA is clustered in the same orthologous group and is 27,34 identical to DaAHT2_0547 and 29,79 % identical to DaAHT2_0420 (Fig. 4a). Only one of the D. alkaliphilus AHT2T phsA/psrA genes is located within an operon of three subunits (Fig. 4a). This means that the D. alkaliphilus AHT2T gene with the locus tag DaAHT2_0420 is most probably the active psrA/phsA. Laboratory culture evidence points towards the D. alkaliphilus AHT2T DaAHT2_4020 – DaAHT2_0418 operon being functional as a sulfur reductase, as it is unable to grow on thiosulfate in absence of H2 as electron donor [3]. In addition, the operon is directly adjacent to a sulfur transferase rhodanese domain (DaAHT2_0417), which has been suggested to be essential for the binding, stabilizing and transferring sulfur to the psrA subunit [32]. However, more research is needed to define this gene operon as either a psr or a phs gene cluster.
Fig. 4
Fig. 4

A comparison of the thiosulfate reductase (phs) and sulfur reductase (psr) gene annotation. a The phs (grey) and psr (yellow) gene clusters and how similar they are to a phs/psr gene cluster in D. alkaliphilus AHT2T (blue) based on BLAST analysis [47]. b A phylogenetic tree of an orthologous group of the psrA gene derived from EggNOG (ENOG4107QY8) [31]. Sequences annotated as phs are indicated in grey and sequences annotated as psr are coloured in yellow. The orthologous genes in D. alkaliphilus AHT2T are coloured in blue, and white with a blue outline

Adaptations to the haloalkaline environment

There are several adaptations that haloalkaliphiles can use to survive in the haloalkaline environment: bioenergetic adaptations, structural membrane adaptations and the use of osmoprotectants to retain osmotic balance [1]. The genome of D. alkaliphilus AHT2T contains a voltage gated sodium channel gene ncbA (DaAHT2_0077) and the electrogenic sodium/proton antiporter mrpBCDEFG operon (DaAHT2_2362 to DaAHT2_2357). The nqr operon encodes a sodium pumping NADH: quinone oxidoreductase (alternative to H+-pumping conventional NADH-quionone oxidoreductases) that shuttles electrons from NADH to ubiquinone [33, 34]. The D. alkaliphilus AHT2T genome contains the first account of the nqr operon in anaerobic haloalkaliphiles [35, 36]. The locus tags of the nqr gene cluster nqrA-nqrF in D. alkaliphilus AHT2T are DaAHT2_0042 – DaAHT2_0047, and we also found this cluster in D. alkaliphilus AHT2T’s closest sequenced relative delta proteobacterium sp. MLMS-1 (mldDRAFT_0493-0498) (Fig. 5). The D. alkaliphilus AHT2T genome does not contain genes for the synthesis of ectoine or betaine, which function as common osmoprotectants in haloalkaliphiles, but it does have a choline/betaine transporter (DaAHT2_1056).
Fig. 5
Fig. 5

The sodium dependent NADH ubiquinone oxidoreductase (nqr) gene cluster. Vibrio alginolyticus ATCC 17749T [33, 48] was used as a reference for the delta proteobacterium sp. MLMS-1 and D. alkaliphilus AHT2T gene clusters


In this manuscript we give a short description of the D. alkaliphilus AHT2T genome, which was isolated from hypersaline soda lake sediments in the Libyan Desert in Egypt. Its ability to perform inorganic sulfur disproportionation reactions in laboratory cultures indicates that the necessary gene pathways are present in the genome of this organism. The metabolic pathways of disproportionation are so far poorly understood; therefore, further investigation of the D. alkaliphilus AHT2T genome may lead to insights which genes are essential to this metabolism. In addition, a more in depth genome sequence analysis might provide more insights into autotrophic carbon metabolism in haloalkaline environments.



Carbon monoxide dehydrogenase


Acetyl-CoA synthase


Corrinoid iron-sulfur protein large subunit

Formate DH

Formate dehydrogenase


Formyl-H4-folate synthase


Formyl-H4folate cyclohydrolase/methylene-H4folate dehydrogenase


Methylene-H4folate reductase/corrinoid iron-sulfur protein small subunit fusion


Type II secretory pathway ATPase PulE




Wood Ljungdahl



Emily Denise Melton, Lex Overmars and Gerard Muyzer are supported by ERC Advanced Grant PARASOL (No. 322551); Dimitry Y. Sorokin was supported by the Gravitation SIAM grant 24002002 and the RFBR grant 16-04-00035. Alla L. Lapidus is supported by the RSF grant 14-50-00069. The work conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, was supported under Contract No. DE-AC02-05CH11231.

Authors’ contributions

EDM drafted and wrote the manuscript. DYS, LO, GM, NCK and ALL contributed to the written manuscript. DYS, LO and GM stimulated critical discussions. DS cultured D. alkaliphilus and extracted the DNA. The sequencing and annotation of the genome were performed at the JGI by OC, AC, MP, NI, NS, NCK, TW and all. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (, which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

Microbial Systems Ecology, Department of Aquatic Microbiology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands
Winogradsky Institute of Microbiology, Research Centre of Biotechnology, RAS, Moscow, Russia
Department of Biotechnology, Delft University of Technology, Delft, The Netherlands
Bioscience Division, Department of Energy Joint Genome Institute, Los Alamos National Laboratory, Los Alamos, NM 87545, USA
Joint Genome Institute, Walnut Creek, CA, USA
Biological Data Management and Technology Center, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
Department of Biological Sciences, Faculty of Science, King Abdulaziz University, Jeddah, Saudi Arabia
Center for Algorithmic Biotechnology, Institute of Translational Biomedicine, St. Petersburg State University, St. Petersburg, Russia


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