Skip to main content
  • Short genome report
  • Open access
  • Published:

High-quality draft genome sequence of Sedimenticola selenatireducens strain AK4OH1T, a gammaproteobacterium isolated from estuarine sediment

Abstract

Sedimenticola selenatireducens strain AK4OH1T (= DSM 17993T = ATCC BAA-1233T) is a microaerophilic bacterium isolated from sediment from the Arthur Kill intertidal strait between New Jersey and Staten Island, NY. S. selenatireducens is Gram-negative and belongs to the Gammaproteobacteria. Strain AK4OH1T was the first representative of its genus to be isolated for its unique coupling of the oxidation of aromatic acids to the respiration of selenate. It is a versatile heterotroph and can use a variety of carbon compounds, but can also grow lithoautotrophically under hypoxic and anaerobic conditions. The draft genome comprises 4,588,530 bp and 4276 predicted protein-coding genes including genes for the anaerobic degradation of 4-hydroxybenzoate and benzoate. Here we report the main features of the genome of S. selenatireducens strain AK4OH1T.

Introduction

Selenium (Se) is an intriguing element in that microbes actively metabolize it through reduction, oxidation, methylation and demethylation reactions, using some of these to conserve energy. Of particular interest is the process of dissimilatory Se reduction, where the Se oxyanion, selenate [Se(VI)], is sequentially reduced to selenite [Se(IV)] and further to insoluble elemental Se(0). The ability to respire selenate/selenite is comparatively rare, nonetheless, is found in phylogenetically diverse anaerobes [1]. SeRB display a tremendous phylogenetic diversity, and yet the metabolic function seems to be conserved (or alternatively horizontally dispersed) in these unrelated groups. Furthermore, the physiologies of the known selenate-respiring bacteria appear to vary greatly. For example, they are able to couple growth to a wide range of electron acceptors such as arsenate, [2, 3] cobalt oxide (Co(III)) [4], and tellurite [5] to name a few. SeRB have been isolated from a variety of different locations. A few examples are: in California in the San Joaquin Valley [6], from estuarine sediment in NJ [7], from a glass manufacturing plant in Japan [8], and from the dead sea [9].

Sedimenticola selenatireducens type strain AK4OH1T (= DSM 17993T = ATCC BA-1233T ) is a member of the Gammaproteobacteria isolated from estuarine sediment for its unique ability to couple the oxidation of aromatic acids to selenate respiration. The genus Sedimenticola currently includes seven cultivated strains of which two species have been named and described: S. selenatireducens strain AK4OH1T, the type strain of the type species for this genus [10], S. selenatireducens strain CUZ [11], S. thiotaurini strain SIP-G1 [12], Sedimenticola sp. strain Ke4OH1 [7], and Sedimenticola sp. strain NSS [11]. Here we summarize the physiological features of Sedimenticola selenatireducens AK4OH1T and provide a description of its genome.

Organism information

Classification and features

S. selenatireducens strain AK4OH1T was isolated from estuarine sediment in the New York-New Jersey harbor estuary (40°586′N, 74°207′E) [10]. The position of strain AK4OH1T relative to its phylogenetic neighbors is shown in Fig. 1. S. selenatireducens strain CUZ [11] is the closest relative to strain AK4OH1T with a 16S rRNA gene similarity of 100 %, yet interestingly, it has not been found to respire selenate. In addition to these two, there are five other cultivated strains of the genus Sedimenticola : S. thiotaurini strain SIP-G1T [12], Sedimenticola sp. strain NSS [11], and Sedimenticola sp. strain Ke4OH1 [7]. The isolate TT-Z (accession number AM292414) [13] groups among the Sedimenticola strains (Fig. 1) suggesting that it is part of the Sedimenticola genus. The isolate IR (accession number AF521582) groups closely with strain AK4OH1T and strain CUZ, and its position in the phylogenetic tree suggests that it is a member of the Sedimenticola selenatireducens species.

Fig. 1
figure 1

Phylogenetic analysis highlighting the position of Sedimenticola selenatireducens strain AK4OH1T relative to its closest neighbors based on the 16S rRNA gene. The evolutionary history was inferred by using the Maximum Likelihood method based on the Tamura-Nei model [29]. The tree with the highest log likelihood (-3985.1130) is shown. The percentage of trees in which the associated taxa clustered together is shown next to the branches. Initial tree(s) for the heuristic search were obtained by applying the Neighbor-Joining method to a matrix of pairwise distances estimated using the Maximum Composite Likelihood (MCL) approach. The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. The analysis involved 15 nucleotide sequences. All positions containing gaps and missing data were eliminated. There were a total of 1276 positions in the final dataset. Evolutionary analyses were conducted in MEGA6 [30]. The strains and their corresponding GenBank accession numbers for 16S rRNA genes are listed in parentheses. The genome accession number and locus tag of strain AK4OH1T are NZ_ATZE00000000.1 and A3GODRAFT_03746. (T = type strain). Bar: 0.01 substitutions per nucleotide position. C. okenii was used as an outgroup

Cells of strain AK4OH1T are Gram-negative and rod-shaped [10] (Fig. 2 and Table 1). The strain can grow heterotrophically or lithoautotrophically under hypoxic and anaerobic conditions [12]. Motility is observed during early to mid-exponential growth on liquid MB2216 medium, but not in late exponential phase, and cell morphology varies depending on growth conditions [10, 12].

Fig. 2
figure 2

Electron micrograph of cells of S. selenatireducens strain AK4OH1T. Bar, 1 μm

Table 1 Classification and general features of Sedimenticola selenatireducens strain AK4OH1T according to the MIGS recommendations [18]

Strain AK4OH1T is able to utilize benzoate, 3-hydroxybenzoate, 4-hydroxybenzoate, acetate, formate, fumarate, L-lactate, D- and L-malate, pyruvate, methyl-pyruvate, propionate, succinate, methyl-succinate, bromo-succinate, p-hydroxyphenylacetic acid, α-ketoglutaric acid, arabinose, lyxose, ribose, xylose, D-galactonic acid-γ-lactone, α-hydroxy-glutaric acid-γ-lactone, L-alanine, L-glutamic acid, L-serine, tyramine, and phenylethylamine [10, 12].

Chemotaxonomic data

The predominant cellular fatty acids in strain AK4OH1T are C16:0 (61.9 %), C16:1 ω7c (14.4 %), C18:0 (8.4 %), and C18:1 ω7c (7.2 %) [10].

Genome sequencing information

Genome project history

S. selenatireducens strain AK4OH1T was selected for sequencing in 2011 based on its phylogenetic position [14, 15] and is part of the study Genomic Encyclopedia of Type Strains, Phase I: the one thousand microbial genomes project (KMG-I) [16]. The goal of the KMG-I study was to increase the coverage of sequenced reference microbial genomes [17]. The Quality Draft (QD) assembly and annotation were made available for public access on June 18, 2014. Table 2 presents the project information and its association with MIGS version 2.0 compliance [18]. The NCBI accession number for the Bioproject is PRJNA165429. The genome accession number is ATZE00000000.1 consisting of 41 contigs (ATZE01000001-ATZE01000041) and 37 scaffolds.

Table 2 Project information

Growth conditions and genomic DNA preparation

S. selenatireducens strain AK4OH1T was grown in mineral salt medium at 28 °C with 10 mM Na2SeO4 as electron acceptor and 250 μM 4-hydroxybenzoate as carbon source, as previously described [10]. Genomic DNA was isolated from 0.5 g of cell paste using JetFlex Genomic DNA Purification Kit (GENOMED) as recommended by the manufacturer.

Genome sequencing and assembly

Sequencing was achieved using an Illumina [19] platform using a std paired-end library obtaining 273× fold coverage. The sequencing was done at the DOE Joint Genome Institute. ALLPATHS assembly software [20] was used to obtain 41 final contigs. Quality check and assembly statistics were performed at JGI. The raw sequences were screened against contaminants and 0.1 % of the reads were removed.

Genome annotation

Gene calling was performed using Prodigal 2.5 [21]. The genome sequence was analyzed using the Joint Genome Institute IMG system [22]. Ribosomal RNAs were predicted based upon sequence similarity, using BLAST, against the non-redundant nucleotide database and/or using Infernal and Rfam models. tRNA genes were found using tRNAscan-SE [23]. The predicted CDS were searched using the NCBI non-redundant protein database. The major metabolic pathways and predicted protein set were searched using KEGG, SwissProt, COG, Pfam, and InterPro protein databases implemented in the IMG. Additional gene prediction analysis and manual functional annotation were performed within IMG and using Artemis software (release 13.0, Sanger Institute).

Genome properties

The high quality draft genome sequence consists of 37 scaffolds that account for a total of 4,588,530 bp with a 56.6 % G + C content. In total, 4331 genes were predicted, 4276 of which are protein-coding genes, 55 RNA genes, and no pseudogenes. The majority of the predicted genes (79 %) were assigned a predicted function. The properties and statistics of the genome are summarized in Table 3 and Table 4.

Table 3 Genome statistics
Table 4 Number of genes associated with general COG functional categories

Insights from the genome sequence

The respiratory flexibility of anaerobic prokaryotes allowing them to employ different terminal electron acceptors for respiration enables these organisms to thrive in dynamic redox environments. Among the enzymes that catalyze oxidation-reduction reactions of metals and metalloids are those that are highly conserved and belong to the DMSO reductase family [24]. Key members of the DMSO family of reductases, which transfer electrons to a variety of substrates that act as terminal electron acceptors for energy generation, are nitrate reductases (Nar, Nap, Nas), arsenate reductase (Arr), selenate reductase (Ser), and chlorate reductase (Clr), among others.

S. selenatireducens strain AK4OH1T can use nitrate, nitrite and selenate as the terminal electron acceptors for anaerobic growth, while using the electron donors acetate, lactate, pyruvate, benzoate, 3-hydroxybenzoate, and 4-hydroxybenzoate [10]. Chlorate and perchlorate can be used as electron acceptors when peptone is used as an energy source [12]. (Micro-)aerobic growth with oxygen as electron-acceptor and peptones as electron-donor is also detected [12]

Within the AK4OH1T genome, there are several likely DMSO reductases. Figure 3 shows the grouping of AK4OH1T genes with closely matching, known, DMSO reductases. A3GODRAFT_03903 groups closely with the NapA, from Magnetospira sp. QH-2. A3GODRAFT_01428 clusters together with the NarG of Escherichia coli K-12 MG1655. Both of these genes are organized in gene clusters similar to known nap and nar operons [25]. BLAST searches of the AK4OH1T genome using arsenate reductases showed no genes with significant similarity. This agrees with strain AK4OH1’s inability to respire arsenate [10]. A3GODRAFT_02603 and A3GODRAFT_03351 from strain AK4OH1T cluster closely with the chlorate reductase from Diaphorobacter sp. J5-51 and with the selenate reductase from Thauera selenatis . A3GODRAFT_02603, which groups closest with ClrA, resembles the gene organization of a clr operon [26]. While the only well-studied respiratory selenate reductase, serA, is from Thauera selenatis , A3GODRAFT_03351 and its neighboring genes follow the same organization as found with serABDC [27]. Gene A3GODRAFT_04296 clusters together with the perchlorate reductase from Dechloromonas aromatica, and appears to have the same gene organization as a pcr operon [28].

Fig. 3
figure 3

Phylogenetic analysis highlighting the relation of Sedimenticola selenatireducens strain AK4OH1T genes to known DMSO reductases by Maximum Likelihood method. The evolutionary history was inferred by using the Maximum Likelihood method based on the JTT matrix-based model [37]. The tree with the highest log likelihood (-17325.9218) is shown. The percentage of trees in which the associated taxa clustered together is shown next to the branches. Initial tree(s) for the heuristic search were obtained by applying the Neighbor-Joining method to a matrix of pairwise distances estimated using a JTT model. The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. The analysis involved 13 amino acid sequences. All positions containing gaps and missing data were eliminated. There were a total of 724 positions in the final dataset. Evolutionary analyses were conducted in MEGA6 [30]. GenBank accession numbers are listed in parentheses. Bar = 0.5 substitutions per nucleotide position

Conclusions

The complete genome of the estuarine bacterium Sedimenticola selenatireducens AK4OH1T provides a stronger foundation from which to learn more about the process of dissimilatory selenate reduction. As AK4OH1T was the first organism isolated capable of coupling the respiration of selenate to the oxidation of benzoic acids, its genome also provides a starting point for learning more about this unique capability.

Abbreviations

DMSO:

Dimethyl sulfoxide

SeRB:

Selenate reducing bacteria

References

  1. Nancharaiah YV, Lens PNL. Ecology and biotechnology of selenium-respiring bacteria. Microbiol Mol Biol Rev. 2015;79:61–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Laverman AM, Blum JS, Schaefer JK, Phillips E, Lovley DR, Oremland RS. Growth of strain SES-3 with arsenate and other diverse electron acceptors. Appl Environ Microbiol. 1995;61:3556–61.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Rauschenbach I, Posternak V, Cantarella P, McConnell J, Starovoytov V, Häggblom MM. Seleniivibrio woodruffii gen. nov., sp. nov., a selenate- and arsenate-respiring bacterium in the Deferribacteraceae. Int J System Evol Microbiol. 2013;63:3659–65.

    Article  CAS  Google Scholar 

  4. Knight V, Blakemore R. Reduction of diverse electron acceptors by Aeromonas hydrophila. Arch Microbiol. 1998;169:239–48.

    Article  CAS  PubMed  Google Scholar 

  5. Baesman SM, Stolz JF, Kulp TR, Oremland RS. Enrichment and isolation of Bacillus beveridgei sp. nov., a facultative anaerobic haloalkaliphile from Mono Lake, California, that respires oxyanions of tellurium, selenium, and arsenic. Extremophiles. 2009;13:695–705.

    Article  CAS  PubMed  Google Scholar 

  6. Macy J, Rech S, Auling G, Dorsch M, Stackebrandt E, Sly L. Thauera selenatis gen. nov., sp. nov., a member of the beta subclass of Proteobacteria with a novel type of anaerobic respiration. Int J System Bacteriol. 1993;43:135.

    Article  CAS  Google Scholar 

  7. Knight VK, Nijenhuis I, Kerkhof LJ, Häggblom MM. Degradation of aromatic compounds coupled to selenate reduction. Geomicrobiol J. 2002;19:77–86.

    Article  CAS  Google Scholar 

  8. Yamamura S, Yamashita M, Fujimoto N, et al. Bacillus selenatarsenatis sp. nov., a selenate- and arsenate-reducing bacterium isolated from the effluent drain of a glass-manufacturing plant. Int J System Evol Microbiol. 2007;57:1060–4.

    Article  CAS  Google Scholar 

  9. Blum JS, Stolz JF, Oren A, Oremland RS. Selenihalanaerobacter shriftii gen. nov., sp. nov., a halophilic anaerobe from Dead Sea sediments that respires selenate. Arch Microbiol. 2001;175:208–19.

    Article  CAS  PubMed  Google Scholar 

  10. Narasingarao P, Häggblom MM. Sedimenticola selenatireducens, gen. nov., sp. nov., an anaerobic selenate-respiring bacterium isolated from estuarine sediment. Syst Appl Microbiol. 2006;29:382–8.

    Article  CAS  PubMed  Google Scholar 

  11. Carlström CI, Loutey DE, Wang O, et al. Phenotypic and genotypic description of Sedimenticola selenatireducens strain CUZ, a marine (per)chlorate-respiring gammaproteobacterium, and its close relative the chlorate-respiring Sedimenticola strain NSS. Appl Environ Microbiol. 2015;81:2717–26.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Flood BE, Jones DS, Bailey JV. Sedimenticola thiotaurini sp. nov., a sulfide-oxidizing bacterium isolated from salt marsh sediments, and emended description of the genus Sedimenticola and Sedimenticola selenatireducens. Int J Syst Evol Microbiol. 2015;65:2522–30.

    Article  CAS  PubMed  Google Scholar 

  13. Alain K, Harder J, Widdel F, Zengler K. Anaerobic utilization of toluene by marine alpha- and gammaproteobacteria reducing nitrate. Microbiology. 2012;158:2946–57.

    Article  CAS  PubMed  Google Scholar 

  14. Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, et al. A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature. 2009;462:1056–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Göker M, Klenk HP. Phylogeny-driven target selection for large-scale genome sequencing (and other) projects. Stand Genomic Sci. 2013;8:360–74.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Kyrpides NC, Woyke T, Eisen JA, Garrity G, Lilburn TG, Beck BJ, et al. Genomic encyclopedia of type strains, phase I: the one thousand microbial genomes (KMG-I) project. Stand Genomic Sci. 2013;9:628–6234.

    Article  CAS  Google Scholar 

  17. Kyrpides NC, Hugenholtz P, Eisen JA, Woyke T, Göker M, Parker CT, et al. Genomic encyclopedia of Bacteria and Archaea: sequencing a myriad of type strains. PLoS Biol. 2014;8:e1001920.

    Article  Google Scholar 

  18. Field D, Garrity G, Gray T, et al. The minimum information about a genome sequence (MIGS) specification. Nat Biotech. 2008;26:541–7.

    Article  CAS  Google Scholar 

  19. Bennett S. Solexa Ltd. Pharmacogenomics J. 2004;5:433–8.

    Article  Google Scholar 

  20. Butler J, MacCallum I, Kleber M, et al. ALLPATHS: De novo assembly of whole-genome shotgun microreads. Genome Res. 2008;18:810–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics. 2010;11:119.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Markowitz VM, Chen I-MA, Palaniappan K, et al. IMG 4 version of the integrated microbial genomes comparative analysis system. Nucl Acids Res. 2014;42:D560–7.

    Article  CAS  PubMed  Google Scholar 

  23. Lowe TM, Eddy SR. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucl Acids Res. 1997;25:0955–64.

    Article  CAS  Google Scholar 

  24. Rothery RA, Workun GJ, Weiner JH. The prokaryotic complex iron–sulfur molybdoenzyme family. BBA-Biomembranes. 2008;1778:1897–929.

    Article  CAS  PubMed  Google Scholar 

  25. Richardson DJ, Berks BC, Russell DA, Spiro S, Taylor CJ. Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell Mol Life Sci. 2001;58:165–78.

    Article  CAS  PubMed  Google Scholar 

  26. Lindqvist MH, Nilsson T, Sundin P, Rova M. Chlorate reductase is cotranscribed with cytochrome c and other downstream genes in the gene cluster for chlorate respiration of Ideonella dechloratans. FEMS Microbiol Lett. 2015;362:1–6.

    Article  Google Scholar 

  27. Krafft T, Bowen A, Theis F, Macy JM. Cloning and sequencing of the genes encoding the periplasmic-cytochrome B-containing selenate reductase of Thauera selenatis. DNA Seq. 2000;10:365–77.

    Article  CAS  PubMed  Google Scholar 

  28. Bender KS, Shang C, Chakraborty R, Belchik SM, Coates JD, Achenbach LA. Identification, characterization, and classification of genes encoding perchlorate reductase. J Bacteriol. 2005;187:5090–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993;10:512–26.

    CAS  PubMed  Google Scholar 

  30. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol Biol Evol. 2013;30:2725–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. PNAS. 1990;87:4576–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Garrity GM, Bell JA, Lilburn T. Phylum XIV. Proteobacteria phyl. nov. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s manual of systematic bacteriology. Volume 2, Part B. New York: Springer; 2005. p. 1.

  33. Garrity GM, Bell JA, Lilburn T, Class III. Gammaproteobacteria class. nov. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s manual of systematic bacteriology. Volume 2, Part B. New York: Springer; 2005. p. 1.

  34. Euzéby J. Validation of publication of new names and new combinations previously effectively published outside the IJSEM. List no. 106. Int J Syst Evol Microbiol. 2005;55:2235–8.

  35. Euzéby J. List of new names and new combinations previously effectively, but not validly, published. List no. 112. Int J Syst Evol Microbiol. 2006;56:2507–8.

  36. Ashburner M, Ball CA, Blake JA, et al. Gene Ontology: tool for the unification of biology. Nat Genet. 2000;25:25–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 1992;8:275–82.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Evelyne Brambilla at DSMZ for DNA extraction and Marcel Huntemann, Alicia Clum, Manoj Pillay, Krishnaveni Palaniappan, Neha Varghese, Natalia Mikhailova, Dimitrios Stamatis, T.B.K. Reddy, Chew Yee Ngan, Chris Daum, Nicole Shapiro, Victor Markowitz, and Natalia Ivanova at the U.S. Department of Energy Joint Genome Institute for library preparation, sequencing and genome assembling.

This work was funded in part by the New Jersey Agricultural Experiment Station. The work conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. DG was supported by a C-DEBI (Center for Dark Energy Biosphere Investigation) postdoctoral fellowship.

Authors’ contributions

MMH, EB and NY designed the research. PN carried out initial strain characterization. VS provided the electron micrograph. MG, H-PK, EL, NCK and TW sequenced, assembled and annotated the genome. TSL, DG, EB, NY and MMH performed the research. TSL and DG analyzed the data. TSL, DG, EB, NY and MMH wrote the manuscript. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Max M. Häggblom.

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), 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 (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Louie, T.S., Giovannelli, D., Yee, N. et al. High-quality draft genome sequence of Sedimenticola selenatireducens strain AK4OH1T, a gammaproteobacterium isolated from estuarine sediment. Stand in Genomic Sci 11, 66 (2016). https://doi.org/10.1186/s40793-016-0191-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s40793-016-0191-5

Keywords