- Open Access
Complete genome sequence of Desulfobulbus propionicus type strain (1pr3T)
- Ioanna Pagani1,
- Alla Lapidus1,
- Matt Nolan1,
- Susan Lucas1,
- Nancy Hammon1,
- Shweta Deshpande1,
- Jan-Fang Cheng1,
- Olga Chertkov1, 2,
- Karen Davenport1, 2,
- Roxane Tapia1, 2,
- Cliff Han1, 2,
- Lynne Goodwin1, 2,
- Sam Pitluck1,
- Konstantinos Liolios1,
- Konstantinos Mavromatis1,
- Natalia Ivanova1,
- Natalia Mikhailova1,
- Amrita Pati1,
- Amy Chen3,
- Krishna Palaniappan3,
- Miriam Land1, 4,
- Loren Hauser1, 4,
- Yun-Juan Chang1, 4,
- Cynthia D. Jeffries1, 4,
- John C. Detter1, 2,
- Evelyne Brambilla5,
- K. Palani Kannan5,
- Olivier D. Ngatchou Djao6,
- Manfred Rohde6,
- Rüdiger Pukall5,
- Stefan Spring5,
- Markus Göker5,
- Johannes Sikorski5,
- Tanja Woyke1,
- James Bristow1,
- Jonathan A. Eisen1, 7,
- Victor Markowitz3,
- Philip Hugenholtz1, 8,
- Nikos C. Kyrpides1 and
- Hans-Peter Klenk5
- Published: 4 March 2011
Abstract
Desulfobulbus propionicus Widdel 1981 is the type species of the genus Desulfobulbus, which belongs to the family Desulfobulbaceae. The species is of interest because of its great implication in the sulfur cycle in aquatic sediments, its large substrate spectrum and a broad versatility in using various fermentation pathways. The species was the first example of a pure culture known to disproportionate elemental sulfur to sulfate and sulfide. This is the first completed genome sequence of a member of the genus Desulfobulbus and the third published genome sequence from a member of the family Desulfobulbaceae. The 3,851,869 bp long genome with its 3,351 protein-coding and 57 RNA genes is a part of the Genomic Encyclopedia of Bacteria and Archaea project.
Keywords
- anaerobic
- non-motile
- Gram-negative
- chemoorganotroph
- ellipsoidal to lemon-shaped
- non spore-forming
- mesophilic
- Desulfobulbaceae
- GEBA
Introduction
Strain 1pr3T “Lindhorst” (= DSM 2032 = ATCC 33891 = VKM B-1956) is the type strain of the species Desulfobulbus propionicus, which is the type species of the genus Desulfobulbus [1,2]. The genus currently consists of five validly published named species [3]. The genus name is derived from the Neo-Latin word ‘desulfo-’ meaning ‘desulfurizing’ and the Latin word ‘bulbus’ meaning ‘a bulb or an onion’, yielding the ‘onion-shaped sulfate reducer’ [2]. The species epithet is derived from the Neo-Latin word ‘acidum propionicum’ and the Latin suffix ‘-icus’ in the sense of ‘pertaining to’; ‘propionicus’ = ‘pertaining to propionic acid’ [2]. Strain 1pr3T “Lindhorst” was isolated by Fritz Widdel in 1982 from anaerobic mud of a village ditch in Lindhorst near Hannover [4]. Other strains have been isolated from anaerobic mud in a forest pond near Hannover and from a mud flat of the Jadebusen (North Sea) [4], from an anaerobic intertidal sediment in the Ems-Dollard estuary (Netherlands) [5], and from a sulfate-reducing fluidized bed reactor inoculated with mine sediments and granular sludge [6]. Several studies have been carried out on the metabolic pathways of the strain 1pr3T [4,7,8]. Here we present a summary classification and a set of features for D. propionicus strain 1pr3T, together with the description of the complete genomic sequencing and annotation.
Classification and features
A representative genomic 16S rRNA sequence of strain 1pr3T was compared using NCBI BLAST under default settings (e.g., considering only the high-scoring segment pairs (HSPs) from the best 250 hits) with the most recent release of the Greengenes database [9] and the relative frequencies, weighted by BLAST scores, of taxa and keywords (reduced to their stem [10]) were determined. The four most frequent genera were Desulfobulbus (76.1%), Desulfurivibrio (11.9%), Desulforhopalus (8.1%) and Desulfobacterium (3.9%) (19 hits in total). Regarding the eleven hits to sequences from members of the species, the average identity within HSPs was 95.1%, whereas the average coverage by HSPs was 94.7%. Regarding the nine hits to sequences from other members of the genus, the average identity within HSPs was 94.9%, whereas the average coverage by HSPs was 94.9%. Among all other species, the one yielding the highest score was Desulfobulbus elongatus, which corresponded to an identity of 96.9% and an HSP coverage of 93.8%. The highest-scoring environmental sequence was FJ517134 (“semiarid ‘Tablas de Daimiel National Park’ wetland (Central Spain) unraveled water clone TDNP Wbc97 92 1 234′), which showed an identity of 97.8% and a HSP coverage of 98.3%. The five most frequent keywords within the labels of environmental samples which yielded hits were ‘sediment’ (8.4%), ‘marin’ (2.9%), ‘microbi’ (2.5%), ‘sea’ (1.7%) and ‘seep’ (1.7%) (231 hits in total). These keywords are in line with habitats from which the cultivated strains of D. propionicus were isolated. Environmental samples which resulted in hits of a higher score than the highest scoring species were not found.
Phylogenetic tree highlighting the position of D. propionicus relative to the other type strains within the family Desulfobulbaceae. The tree was inferred from 1,425 aligned characters [11,12] of the 16S rRNA gene sequence under the maximum likelihood criterion [13] and rooted in accordance with the current taxonomy. The branches are scaled in terms of the expected number of substitutions per site. Numbers above branches are support values from 200 bootstrap replicates [14] if larger than 60%. Lineages with type strain genome sequencing projects registered in GOLD [15] are shown in blue, published genomes [16] in bold.
Scanning electron micrograph of D. propionicus 1pr3T
Classification and general features of D. propionicus 1pr3T according to the MIGS recommendations [17].
MIGS ID | Property | Term | Evidence code |
---|---|---|---|
Current classification | Domain Bacteria | TAS [18] | |
Phylum Proteobacteria | TAS [19] | ||
Class Deltaproteobacteria | |||
Order Desulfobacterales | |||
Family Desulfobulbaceae | |||
Genus Desulfobulbus | |||
Species Desulfobulbus propionicus | |||
Type strain 1pr3 | TAS [4] | ||
Gram stain | negative | TAS [4] | |
Cell shape | ellipsoidal to lemon-shaped | TAS [4] | |
Motility | non-motile | TAS [4] | |
Sporulation | none | TAS [4] | |
Temperature range | 10°C–43°C | TAS [4] | |
Optimum temperature | 39°C | TAS [4] | |
Salinity | not reported | NAS | |
MIGS-22 | Oxygen requirement | anaerobic | TAS [4] |
Carbon source | propionate, lactate, ethanol, propanol, pyruvate | ||
Energy source | chemoorganotroph | TAS [4] | |
MIGS-6 | Habitat | anaerobic freshwater sediments | TAS [24] |
MIGS-15 | Biotic relationship | not reported | NAS |
MIGS-14 | Pathogenicity | not reported | NAS |
Biosafety level | 1 | TAS [25] | |
Isolation | anaerobic mud | TAS [4] | |
MIGS-4 | Geographic location | Lindhort near Hannover, Germany | TAS [4] |
MIGS-5 | Sample collection time | 1980 or before | NAS |
MIGS-4.1 | Latitude | 52.38 | NAS |
MIGS-4.2 | Longitude | 9.82 | NAS |
MIGS-4.3 | Depth | not reported | NAS |
MIGS-4.4 | Altitude | not reported | NAS |
Chemotaxonomy
Odd-chain fatty acids predominated in the fatty acid profile of the strain 1pr3T (77% of the total fatty acids vs. 23% for the even-chain fatty acids) [35,36], reflecting the use of propionate as a chain initiator for fatty acid biosynthesis [35]. The major fatty acids, when grown on propionate, were found to be C17:1ω6 (51.5%), C15:0 (28.3%), C16:0 (6.9%), C14:0 (5.2%), C18:0 (3.1%), C15:1 ω6 and C16:1 ω5, (2.4% each) and C18:1 ω7 (2.1%). The minor fatty acids were C17:0 (0.6% of the total fatty acids), C16:1 ω7 (0.9%), C18:1 ω9 and C15:1Δ7 (1.0% each), C12:0 (1.3%), C17:1 ω8 (1.6%) and C13:0 (1.7%) [36].
Genome sequencing and annotation
Genome project history
Genome sequencing project information
MIGS ID | Property | Term |
---|---|---|
MIGS-31 | Finishing quality | Finished |
MIGS-28 | Libraries used | Three genomic libraries:one 454 pyrosequence standard library, one 454 PE library (12 kb insert size), one Illumina library |
MIGS-29 | Sequencing platforms | Illumina GAii, 454 GS FLX Titanium |
MIGS-31.2 | Sequencing coverage | 109.7 × Illumina; 37.9 × pyrosequence |
MIGS-30 | Assemblers | Newbler version 2.0.00.20-PostRelease-11-05-2008-gcc-3.4.6, Velvet, phrap |
MIGS-32 | Gene calling method | Prodigal 1.4, GenePRIMP |
INSDC ID | CP002364 | |
Genbank Date of Release | January 28, 2011 | |
GOLD ID | Gc01599 | |
NCBI project ID | 32577 | |
Database: IMG-GEBA | 2503538026 | |
MIGS-13 | Source material identifier | DSM 2032 |
Project relevance | Tree of Life, GEBA |
Growth conditions and DNA isolation
D. propionicus 1pr3T, DSM 2032, was grown anaerobically in DSMZ medium 194 (Desulfobulbus medium) [39] at 37°C. DNA was isolated from 0.5–1 g of cell paste using MasterPure Gram-positive DNA purification kit (Epicentre MGP04100) following the standard protocol as recommended by the manufacturer, with modification st/LALM for cell lysis as described in Wu et al. [38]. DNA is available through the DNA Bank Network [40,41].
Genome sequencing and assembly
The genome was sequenced using a combination of Illumina and 454 sequencing platforms. All general aspects of library construction and sequencing can be found at the JGI website [42]. Pyrosequencing reads were assembled using the Newbler assembler version 2.0.00.20-PostRelease-11-05-2008-gcc-3.4.6 (Roche). The initial Newbler assembly consisting of 35 contigs in two scaffolds was converted into a phrap [43] assembly by making fake reads from the consensus, to collect the read pairs in the 454 paired end library. Illumina GAii sequencing data (327Mb) was assembled with Velvet [44] and the consensus sequences were shredded into 1.5 kb overlapped fake reads and assembled together with the 454 data. The 454 draft assembly was based on 145.0 Mb 454 draft data and all of the 454 paired end data. Newbler parameters are -consed -a 50 -l 350 -g -m -ml 20. The Phred/Phrap/Consed software package [43] was used for sequence assembly and quality assessment in the subsequent finishing process. After the shotgun stage, reads were assembled with parallel phrap (High Performance Software, LLC). Possible mis-assemblies were corrected with gapResolution [42], Dupfinisher [45], or sequencing cloned bridging PCR fragments with subcloning or transposon bombing (Epicentre Biotechnologies, Madison, WI). Gaps between contigs were closed by editing in Consed, by PCR and by Bubble PCR primer walks (J.-F.Chang, unpublished). A total of 563 additional reactions and five shatter libraries were necessary to close gaps and to raise the quality of the finished sequence. Illumina reads were also used to correct potential base errors and increase consensus quality using a software Polisher developed at JGI [46]. The error rate of the completed genome sequence is less than 1 in 100,000. Together, the combination of the Illumina and 454 sequencing platforms provided 147.6 × coverage of the genome. The final assembly contained 475,513 pyrosequence and 11,740,513 Illumina reads.
Genome annotation
Genes were identified using Prodigal [47] as part of the Oak Ridge National Laboratory genome annotation pipeline, followed by a round of manual curation using the JGI GenePRIMP pipeline [48]. The predicted CDSs were translated and used to search the National Center for Biotechnology Information (NCBI) nonredundant database, UniProt, TIGR-Fam, Pfam, PRIAM, KEGG, COG, and InterPro databases. Additional gene prediction analysis and functional annotation was performed within the Integrated Microbial Genomes - Expert Review (IMG-ER) platform [49].
Genome properties
Graphical circular map of the chromosome. From outside to the center: Genes on forward strand (color by COG categories), Genes on reverse strand (color by COG categories), RNA genes (tRNAs green, rRNAs red, other RNAs black), GC content, GC skew.
Genome Statistics
Attribute | Value | % of Total |
---|---|---|
Genome size (bp) | 3,851,869 | 100.00% |
DNA coding region (bp) | 3,410,010 | 88.53% |
DNA G+C content (bp) | 2,269,813 | 58.93% |
Number of replicons | 1 | |
Extrachromosomal elements | 0 | |
Total genes | 3,408 | 100.00% |
RNA genes | 57 | 1.67% |
rRNA operons | 2 | |
Protein-coding genes | 3,351 | 98.33% |
Pseudo genes | 68 | 2.00% |
Genes with function prediction | 2,402 | 70.48% |
Genes in paralog clusters | 492 | 14.44% |
Genes assigned to COGs | 2,502 | 73.42% |
Genes assigned Pfam domains | 2,623 | 76.97% |
Genes with signal peptides | 1,073 | 31.48% |
Genes with transmembrane helices | 812 | 23.83% |
CRISPR repeats | 1 |
Number of genes associated with the general COG functional categories
Code | value | %age | Description |
---|---|---|---|
J | 155 | 5.6 | Translation, ribosomal structure and biogenesis |
A | 1 | 0.1 | RNA processing and modification |
K | 128 | 4.6 | Transcription |
L | 154 | 5.6 | Replication, recombination and repair |
B | 5 | 0.2 | Chromatin structure and dynamics |
D | 28 | 1.0 | Cell cycle control, cell division, chromosome partitioning |
Y | 0 | 0.0 | Nuclear structure |
V | 45 | 1.6 | Defense mechanisms |
T | 297 | 10.8 | Signal transduction mechanisms |
M | 184 | 6.7 | Cell wall/membrane/envelope biogenesis |
N | 106 | 3.8 | Cell motility |
Z | 0 | 0.0 | Cytoskeleton |
W | 0 | 0.0 | Extracellular structures |
U | 83 | 3.0 | Intracellular trafficking and secretion, and vesicular transport |
O | 106 | 3.8 | Posttranslational modification, protein turnover, chaperones |
C | 274 | 9.9 | Energy production and conversion |
G | 96 | 3.5 | Carbohydrate transport and metabolism |
E | 185 | 6.7 | Amino acid transport and metabolism |
F | 66 | 2.4 | Nucleotide transport and metabolism |
H | 145 | 5.3 | Coenzyme transport and metabolism |
I | 74 | 2.7 | Lipid transport and metabolism |
P | 123 | 4.5 | Inorganic ion transport and metabolism |
Q | 40 | 1.5 | Secondary metabolites biosynthesis, transport and catabolism |
R | 274 | 9.9 | General function prediction only |
S | 195 | 7.1 | Function unknown |
- | 906 | 26.6 | Not in COGs |
Declarations
Acknowledgements
We would like to gratefully acknowledge the help of Katja Steenblock (DSMZ) for growing D. propionicus cultures. 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, as well as German Research Foundation (DFG) INST 599/1-2.
Authors’ Affiliations
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