Abstract
This genome report describes the draft genome and the physiological characteristics of Desulfitobacterium hafniense PCE-S, a Gram-positive bacterium known to dechlorinate tetrachloroethene (PCE) to dichloroethene by a PCE reductive dehalogenase. The draft genome has a size of 5,666,696 bp with a G + C content of 47.3%. The genome is very similar to the already sequenced Desulfitobacterium hafniense Y51 and the type strain DCB-2. We identified two complete reductive dehalogenase (rdh) genes in the genome of D. hafniense PCE-S, one of which encodes PceA, the PCE reductive dehalogenase, and is located on a transposon. Interestingly, this transposon structure differs from the PceA-containing transposon of D. hafniense Y51. The second rdh encodes an unknown reductive dehalogenase, highly similar to rdhA 7 found in D. hafniense DCB-2, in which the corresponding gene is disrupted. This reductive dehalogenase might be responsible for the reductive dechlorination of 2,4,5-trichlorophenol and pentachlorophenol, which is mediated by D. hafniense PCE-S in addition to the reductive dechlorination of PCE.
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Introduction
Desulfitobacterium spp. are anaerobic Gram-positive bacteria belonging to the phylum Firmicutes. Desulfitobacteria are metabolically versatile bacteria capable of utilizing a wide range of electron donors and acceptors, the latter also including organohalides. Previously, the genome sequences of Desulfitobacterium hafniense Y51 and DCB-2 have been published [1, 2], and further genomes of various desulfitobacteria are expected to be published in the near future as the result of ongoing sequencing projects (Kruse et al, unpublished results). The genomes of Desulfitobacterium hafniense DCB-2 and Y51 are relatively large (5.3 and 5.7 Mbp, respectively) and are characterized by a high number of genes related to energy metabolism. In both genomes, at least one gene encoding a reductive dehalogenase was found. D. hafniense DCB-2 contains seven rdh genes, two of which are likely non-functional due to either a transposase insertion or a frameshift mutation. The D. hafniense Y51 genome harbours one reductive dehalogenase gene, encoding a PCE reductive dehalogenase [1]. Despite the great interest in the potential application of Desulfitobacterium spp. and other organohalide-respiring bacteria for bioremediation, only a few reductive dehalogenases have been biochemically characterized. One example of a well-studied reductive dehalogenase is the tetrachloroethene reductase, PceA, from D. hafniense PCE-S [3–6].
Here, we describe the isolation and characterization of D. hafniense PCE-S together with its draft genome sequence. The organism is capable of dechlorinating PCE via TCE to cis-DCE as well as of several chlorophenols. The draft genome is 5,666,696 bp in size and is compared to the genome sequences of D. hafniense Y51 and DCB-2. In addition, some morphological and physiological characteristics of strain PCE-S are given and compared to those of other members of the Desulfitobacterium genus.
Organism information
Characterization and features
Desulfitobacterium hafniense (Figure 1) PCE-S was isolated from a fixed-bed reactor inoculated with a methanogenic mixed culture, enriched from soil of a dumping site contaminated with chlorinated ethenes. For further enrichment, the mixed culture was immobilized in a fixed-bed reactor with anoxic mineral medium supplemented with 20 mmol l-1 ethanol and 0.4 to 0.5 mmol l-1 PCE. A pure culture was obtained by inoculating agar medium in roll tubes with a diluted suspension of the biofilm. D. hafniense PCE-S has been deposited in the German Collection of Microorganisms and Cell Cultures (DSM 14645).
D. hafniense PCE-S is a slightly curved, sporulating Gram-positive rod of 0.6 μm (diameter) by 6.0 μm (length). Motility was observed only during exponential growth. The cells are surrounded by a slime sacculus, a trait that distinguishes D. hafniense PCE-S from D. hafniense Y51 (Figure 2). Cytochromes b and c as well as corrinoids, the latter being an essential cofactor of reductive dehalogenases, were detected in strain PCE-S.
D. hafniense PCE-S was shown to utilize pyruvate and several O-methylated compounds (Table 1, [8, 9]) as electron donor, whereas acetate, glucose, fructose, mannitol or sorbitol were not utilized as electron donor. Fumarate, nitrate, thiosulfate and several chlorinated compounds were used as electron acceptors (Table 1). In addition, fermentation of pyruvate as sole energy substrate supports growth of D. hafniense PCE-S. Growth in liquid media was observed at temperatures ranging from 20°C to 45°C with an optimum at 37°C (Table 1). With pyruvate as electron donor and PCE as electron acceptor, the maximal dechlorination rate was observed at pH 7.7.
With PCE as electron acceptor (20 mM, supplied from a hexadecane phase), pyruvate was oxidized to acetate and PCE was dechlorinated to cis,1,2-dichloroethene as the main dechlorination product (≥95%) and minor amounts of trichloroethene (≤5%). The chlorinated ethenes were determined gas chromatographically with N2 as carrier gas using two bonded-phase fused silica capillary columns.
The generation time of growth with pyruvate as electron donor and PCE as electron acceptor was 10 h without and 8 h with 0.1% yeast extract at 30°C. Fumarate as electron acceptor plus yeast extract led to a slightly shorter generation time (7 h) than with PCE/yeast extract.
The ability of D. hafniense PCE-S to dechlorinate polychlorinated phenols was investigated with pyruvate as electron donor and 0.1% yeast extract. Chlorophenols were analysed by HPLC using an RP-18 (5 μm) LiChrospher 100 column (Merck, Darmstadt, Germany). Pentachlorophenol and 2,4,5-trichlorophenol at a concentration of 20 μmol l-1 in mineral medium were dechlorinated. 2,4,5-trichlorophenol was partially dechlorinated to 3,4-dichlorophenol, pentachlorophenol was partially dechlorinated to 3,4-dichlorophenol and an unidentified tetrachlorophenol. 2,6-dichlorophenol, 3,5-dichlorophenol, and 2,4-dichlorophenol were not dechlorinated by D. hafniense PCE-S.
D. hafniense PCE-S has an average nucleotide identity (ANI) of 98.25% to D. hafniense Y51 and of 97.6 to the D. hafniense type strain DCB-2 [1, 2, 19].
Genome sequencing information
Genome project history
The genome consists of 101 contigs in 24 scaffolds, of which the largest scaffold consists of 5,594,916 bp, covering more than 98% of the genome and more than 98% of the protein coding genes. Table 2 presents the project information and its association with MIGS version 2.0 compliance [20].
Growth conditions and DNA preparation
D. hafniense PCE-S was cultivated under anoxic conditions as described by Scholz-Muramatsu et al. [21] and Reinhold et al. [22]. For isolation of genomic DNA, D. hafniense PCE-S was cultivated for one subculture with fumarate after regularly being cultivated in the presence of PCE. The isolation was carried out as described by Reinhold et al. Approximately 12 μg of genomic DNA were used for genome sequencing. The genome sequence of Desulfitobacterium hafniense PCE-S has been deposited in the EMBL database under accession numbers LK996017-LK996040.
Genome sequencing and annotation
DNA was sequenced at GATC Biotech (Konstanz, Germany) on an Illumina MiSeq Personal Sequencer, generating 1,242,269 paired end reads with a length of 250 bp.
Genome size was estimated prior to assembly using kmer spectrumanalyzer .
The assembly was done in parallel with two different assemblers. One assembly was performed with Edena [23], with standard parameters, the second assembly with Ray, using a kmer-value of 125 [24]. Afterwards both assemblies were merged with Zorro with one of the paired end files supplied [25]. Next, this hybrid assembly was scaffolded with opera version 1.2 [26], which was set up to use Bowtie version 0.12.7 for mapping [27]. As last step, Pilon version 1.4 was used for quality assurance on the assembly [28]. Reads were mapped with Bowtie2 version 2.0.6 [29], further converted with Samtools version 0.1.18 (r982:295) [30] , and then provided to Pilon as input data.
All steps were done using standard parameters, unless stated otherwise. Before annotation, the genome was blasted [31] against itself with an e-value of 0.0001. All contigs with a length of less than 500 bp were discarded, as well as those with less than 1,000 bp which matched onto another genomic location with 100% identity.
After annotation, a check for technical duplications was performed. Contigs, which were determined to be such duplications, were manually removed from the initial assembly and replaced with contigs from the second assembler. The assembly workflow was repeated until no more technical duplications were found.
The assembly was then further scaffolded with CONTIGuator version 2.7.4 [32] and the genome of Desulfitobacterium hafniense Y51 as reference [1]. Disagreements with the reference genome were examined with Mauve [33] and Tablet [34], and in case of considerable drops of coverage, the contigs and related reads were isolated, and a re-assembly was performed with Edena. This re-assembly was again scaffolded with CONTIGuator using Y51 as reference genome. Non-scaffolded contigs were included as single contigs in the final result, unless they had a blast hit of more than 90% of their length with a minimum sequence identity of 90% to the scaffold result from CONTIGuator.
The annotation was carried out with an in-house pipeline. In short, this pipeline includes Prodigal version 2.5 for open reading frame identification [35], InterproScan version 5RC7 for protein annotation [36], tRNAscan SE 1.3.1 for tRNA identification [37] and rnammer 1.2 for the prediction of rRNAs [38]. Additional protein function predictions were derived via BLAST [39] UniRef50 and [40] Swissprot databases (downloaded August 2013) [41]. After the annotation process, EC numbers were added with PRIAM version March 06, 2013 [42]. COG assignments were created via blastp best bidirectional hit assignments [43].
Genome properties
The genome consists of 24 scaffolds of 5,666,696 bp (47.3% GC content) and an N50 of 5,594,916 bp. In total, 5,494 genes were predicted, 5,417 of which are (Figure 3) protein-coding genes. 4569 of protein coding genes were assigned to a putative function with the remaining annotated as hypothetical proteins. The properties and the statistics of the genome are summarized in Tables 3, 4 and (Additional file 1: Table S1).
Insights from the genome sequence
Orthologs to other Desulfitobacterium species were determined via bidirectional BLAST hits [43] with at least 70% sequence identity and similar size of both sequences (+/- 5%).
Two reductive dehalogenase genes (DPCES_1664 and DPCES_3087) are encoded on the genome of D. hafniense PCE-S. The latter is the characterized PCE reductive dehalogenase PceA [3]. It is 97% identical (amino acid sequence) to PceA (DSY_2839) from D. hafniense Y51, which is located on a transposon. This transposon structure is also found in D. hafniense TCE1, where it has been shown to be rapidly lost when the organism is grown in the absence of PCE, leading to the loss of the ability to dechlorinate PCE [45]. The transposon containing pceA of D. hafniense PCE-S shows a different structure than the one of D. hafniense Y51 and TCE1 (Figure 4).
Despite the different organization of this transposon, D. hafniense PCE-S also loses the ability to dechlorinate PCE after prolonged cultivation in the absence of PCE [15]. The second reductive dehalogenase gene (DPCES_1664) has no ortholog in Y51. A truncated ortholog is encoded in DCB-2 (Dhaf_2620). In D. hafniense DCB-2, the corresponding rdhA gene is truncated n-terminally (50 amino acids) due to the insertion of a stop codon through a frameshift mutation. It seems likely that the gene product of DPCES_1664 is responsible for the partial dechlorination of pentachlorophenol and 2,4,5-trichlorophenol by D. hafniense PCE-S.
Of the 5,417 protein coding sequences found in the genome of D. hafniense PCE-S, 4,402 are orthologous to proteins encoded in either Y51 or DCB-2. D. hafniense PCE-S harbours six putative phage regions, of which one was classified as a complete prophage, as detected by PHAST [46]. This is opposed to D. hafniense DCB-2 or Y51, where four (DCB-2) and three (Y51) prophages were identified by PHAST as incomplete or questionable, but none as complete. The complete prophage found in D. hafniense PCE-S shows highest similarities to Vibrio phage X29 (NCBI RefSeq accession no. NC_024369). Several enzymes, of which orthologs fulfill a catabolic function, are not encoded in D. hafniense Y51 and DCB-2, but found on the genome of D. hafniense PCE-S: An ethanolamine ammonia lyase system (PCES_2016-2020), three molybdopterin oxidoreductase gene clusters (DPCES_4294-6, DPCES_4565-7, DPCES_4582-4), together with a molybdopterin import cluster (DPCES_0024-6), and a protein annotated as cellulose synthase (DPCES_2599). A cluster encoding polysaccharide synthesis enzymes (DPCES_3251 to 3245) might be responsible for the biosynthesis of the slime sacculus of PCE-S.
Five CRISPR regions with a length from 958 to 3415 bp and 14 to 51 spacers were identified in the genome of D. hafniense PCE-S with CRISPR finder [47]. This is similar to the situation in DCB-2, where five CRISPR regions with a length of 7 to 60 spacers were found, and in Y51, where five CRISPR regions with a length of 12 to 47 spacers were found. The CRISPR regions in all Desulfitobacterium spp. genomes are located in close proximity to each other, separated by not more than 30 kb which are to a large extent covered by CRISPR associated (CAS) proteins.
Conclusions
Taken together, the genome sequence of Desulfitobacterium hafniense PCE-S expands our view on these environmentally interesting microorganisms. The genome sequence gives us insight into the putative chlorophenol dechlorinating activity of a reductive dehalogenase not studied before and might aid bioremediation of chlorinated phenols in the future.
Abbreviations
- PCE:
-
Perchloroethylene or tetrachloroethene
- TCE:
-
Trichloroethene
- DCE:
-
cis-1,2-dichloroethene.
References
Nonaka H, Keresztes G, Shinoda Y, Ikenaga Y, Abe M, Naito K, et al.: Complete genome sequence of the dehalorespiring bacterium Desulfitobacteriumhafniense Y 51 and comparison with Dehalococcoides ethenogenes 195. J Bacteriol 2006, 188:2262–74. 10.1128/JB.188.6.2262-2274.2006
Kim SH, Harzman C, Davis JK, Hutcheson R, Broderick JB, Marsh TL, et al.: Genome sequence of Desulfitobacterium hafniense DCB-2, a Gram-positive anaerobe capable of dehalogenation and metal reduction. BMC Microbiol 2012, 12:21. 10.1186/1471-2180-12-21
Miller E, Wohlfarth G, Diekert G: Purification and characterization of the tetrachloroethene reductive dehalogenase of strain PCE-S. Arch Microbiol 1998, 169:497–502. 10.1007/s002030050602
Ye L, Schilhabel A, Bartram S, Boland W, Diekert G: Reductive dehalogenation of brominated ethenes by Sulfurospirillum multivorans and Desulfitobacterium hafniense PCE-S. Environ Microbiol 2010, 12:501–9. 10.1111/j.1462-2920.2009.02093.x
Cichocka D, Siegert M, Imfeld G, Andert J, Beck K, Diekert G, et al.: Factors controlling the carbon isotope fractionation of tetra- and trichloroethene during reductive dechlorination by Sulfurospirillum ssp. and Desulfitobacterium sp. strain PCE-S. FEMS Microbiol Ecol 2007, 62:98–107. 10.1111/j.1574-6941.2007.00367.x
Miller E, Wohlfarth G, Diekert G: Comparative studies on tetrachloroethene reductive dechlorination mediated by Desulfitobacterium sp. strain PCE-S. Arch Microbiol 1997, 168:513–9. 10.1007/s002030050529
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. 10.1093/molbev/mst197
Neumann A, Engelmann T, Schmitz R, Greiser Y, Orthaus A, Diekert G: Phenyl methyl ethers: novel electron donors for respiratory growth of Desulfitobacterium hafniense and Desulfitobacterium sp strain PCE-S. Arch Microbiol 2004, 181:245–9. 10.1007/s00203-004-0651-y
Mingo FS, Studenik S, Diekert G: Conversion of phenyl methyl ethers by Desulfitobacterium spp. and screening for the genes involved. FEMS Microbiol Ecol 2014.
Woese CR, Kandler O, Wheelis ML: Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A 1990, 87:4576–4579. 10.1073/pnas.87.12.4576
Gibbons N, Murray R: Proposals concerning the higher taxa of bacteria. Int J Syst Evol Microbiol 1978, 28:1–6.
List no. 132: List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 2010, 60:469–472.
Rainey FA: Class II. Clostridia class nov. In In Bergey's Manual of Systematic Bacteriology.. Vol. 3. 2 edition. Edited by: De Vos P, Garrity G, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer KH, Whitman WB. New York: Springer Verlag; 2009:736.
Skerman V, Mcgowan V, Sneath P: Approved lists of bacterial names. Int J Syst Evol Microbiol 1980, 30:225–420.
Rogosa M: Peptococcaceae, a new family to include the Gram-positive, anaerobic cocci of the genera Peptococcus, Peptostreptococcus and Ruminococcus. Int J Syst Bacteriol 1971, 21:234–237. 10.1099/00207713-21-3-234
Utkin I, Woese C, Wiegel J: Isolation and characterization of Desulfitobacterium dehalogenans gen. nov., sp. nov., an anaerobic bacterium which reductively dechlorinates chlorophenolic compounds. Int J Syst Bacteriol 1994, 44:612–9. 10.1099/00207713-44-4-612
Christiansen N, Ahring B: Desulfitobacterium hafniense sp nov, an anaerobic, reductively dechlorinating bacterium. Int J Syst Bact 1996, 46:442–8. 10.1099/00207713-46-2-442
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al.: Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000, 25:25–9. 10.1038/75556
Richter M, Rossello-Mora R: Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S 2009, 106:19126–31. 10.1073/pnas.0906412106
Field D, Garrity G, Gray T, Morrison N, Selengut J, Sterk P, et al.: The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol 2008, 26:541–7. 10.1038/nbt1360
Scholz-Muramatsu H, Neumann A, Messmer M, Moore E, Dieker G: Isolation and characterization of Dehalospirillum multivorans gen. nov., sp. nov., a tetrachloroethene-utilizing, strictly anaerobic bacterium. Arch Microbiol 1995, 163:48–56. 10.1007/BF00262203
Reinhold A, Westermann M, Seifert J, von Bergen M, Schubert T, Diekert G: Impact of Vitamin B-12 on Formation of the Tetrachloroethene Reductive Dehalogenase in Desulfitobacterium hafniense Strain Y51. Appl Environ Microbiol 2012, 78:8025–32. 10.1128/AEM.02173-12
Hernandez D, Francois P, Farinelli L, Osteras M, Schrenzel J: De novo bacterial genome sequencing: millions of very short reads assembled on a desktop computer. Genome Res 2008, 18:802–9. 10.1101/gr.072033.107
Boisvert S, Laviolette F, Corbeil J: Ray: simultaneous assembly of reads from a mix of high-throughput sequencing technologies. J Comput Biol 2010, 17:1519–33. 10.1089/cmb.2009.0238
Zorro - The masked assembler. . http://lge.ibi.unicamp.br/zorro/
Gao S, Sung WK, Nagarajan N: Opera: reconstructing optimal genomic scaffolds with high-throughput paired-end sequences. J Comput Biol 2011, 18:1681–91. 10.1089/cmb.2011.0170
Langmead B, Trapnell C, Pop M, Salzberg SL: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25. 10.1186/gb-2009-10-3-r25
Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, et al.: Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement. PLoS ONE 2014,9(11):e112963. doi:10.1371/journal.pone.0112963 10.1371/journal.pone.0112963
Langmead B, Salzberg SL: Fast gapped-read alignment with Bowtie 2. Nat Methods 2012, 9:357–9. 10.1038/nmeth.1923
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al.: The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078–9. 10.1093/bioinformatics/btp352
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic Local Alignment Search Tool. J Mol Biol 1990, 215:403–10. 10.1016/S0022-2836(05)80360-2
Galardini M, Biondi EG, Bazzicalupo M, Mengoni A: CONTIGuator: a bacterial genomes finishing tool for structural insights on draft genomes. Source Code Biol Med 2011, 6:11. 10.1186/1751-0473-6-11
Darling AE, Mau B, Perna NT: ProgressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010, 5:e11147. 10.1371/journal.pone.0011147
Milne I, Stephen G, Bayer M, Cock PJ, Pritchard L, Cardle L, et al.: Using Tablet for visual exploration of second-generation sequencing data. Brief Bioinform 2013, 14:193–202. 10.1093/bib/bbs012
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. 10.1186/1471-2105-11-119
Hunter S, Jones P, Mitchell A, Apweiler R, Attwood TK, Bateman A, et al.: InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res 2012, 40:D306–312. 10.1093/nar/gkr948
Lowe TM, Eddy SR: Trnascan-SE - a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997,25(5):0955–964. doi:10.1093/nar/25.5.0955 10.1093/nar/25.5.0955
Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW: RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007, 35:3100–8. 10.1093/nar/gkm160
Suzek BE, Huang H, McGarvey P, Mazumder R, Wu CH: UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics 2017, 23:1282–1288.
UniProt-Consortium: Activities at the universal protein resource (UniProt). Nucleic Acids Res 2014, 42:D191-D198.
Morgat A, Coissac E, Coudert E, Axelsen KB, Keller G, Bairoch A, et al.: UniPathway: a resource for the exploration and annotation of metabolic pathways. Nucleic Acids Res 2012, 40:D761–769. 10.1093/nar/gkr1023
Claudel-Renard C, Chevalet C, Faraut T, Khan D: Enzyme-specific profiles for genome annotation - PRIAM. Nucleic Acids Reseach 2003, 31:6633–9. 10.1093/nar/gkg847
Overbeek R, Fonstein M, D'Souza M, Pusch GD, Maltsev N: The use of gene clusters to infer functional coupling. Proc Natl Acad Sci U S A 1990, 96:2896–901.
Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA: BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011, 12:402. 10.1186/1471-2164-12-402
Duret A, Holliger C, Maillard J: The Physiological Opportunism of Desulfitobacterium hafniense Strain TCE1 towards Organohalide Respiration with Tetrachloroethene. Appl Environ Microbiol 2012, 78:6121–7. 10.1128/AEM.01221-12
Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS: PHAST: a fast phage search tool. Nucleic Acids Res 2011, 39:W347–352. 10.1093/nar/gkr485
Grissa I, Vergnaud G, Pourcel C: CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 2007, 35:W52–57. 10.1093/nar/gkm360
Acknowledgement
We would like to thank Heidrun Scholz-Muramatsu and Silke Granzow for initial work on isolation and characterization of D. hafniense PCE-S. The work was funded by the German Research Foundation (DFG research unit FOR 1530). Work of HS and TK was financially supported by the EcoLinc Project of the Netherlands Genomics Initiative, as well as the European Community program FP7 (grants KBBE-211684; BACSIN, and KBBE-222625; METAEXPLORE). BH is supported by Wageningen University and the Wageningen Institute for Environment and Climate Research (WIMEK) through the IP/OP program Systems Biology (project KB-17-003.02-023).
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Authors’ contributions
TG and GD initiated and supervised the study. TG, BH and TK drafted the manuscript and annotated the genome. AR conducted the wetlab work, MW performed electron microscopy. BH and PJS worked on genome sequencing and assembly. TG, BH, TK, HS and GD discussed, analyzed the data and revised the manuscript. All authors read and approved the final manuscript
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Goris, T., Hornung, B., Kruse, T. et al. Draft genome sequence and characterization of Desulfitobacterium hafniense PCE-S. Stand in Genomic Sci 10, 15 (2015). https://doi.org/10.1186/1944-3277-10-15
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DOI: https://doi.org/10.1186/1944-3277-10-15