- Open Access
Complete genome sequence of the thermophilic sulfur-reducer Desulfurobacterium thermolithotrophum type strain (BSAT) from a deep-sea hydrothermal vent
- Markus Göker1,
- Hajnalka Daligault2,
- Romano Mwirichia3,
- Alla Lapidus4,
- Susan Lucas4,
- Shweta Deshpande4,
- Ioanna Pagani4,
- Roxanne Tapia2, 4,
- Jan-Fang Cheng4,
- Lynne Goodwin2, 4,
- Sam Pitluck4,
- Konstantinos Liolios4,
- Natalia Ivanova4,
- Konstantinos Mavromatis4,
- Natalia Mikhailova4,
- Amrita Pati4,
- Amy Chen5,
- Krishna Palaniappan5,
- Cliff Han2,
- Miriam Land4, 6,
- Loren Hauser4, 6,
- Chongle Pan4, 6,
- Evelyne-Marie Brambilla1,
- Manfred Rohde7,
- Stefan Spring1,
- Johannes Sikorski1,
- Reinhard Wirth8,
- John C. Detter2, 4,
- Tanja Woyke4,
- James Bristow4,
- Jonathan A. Eisen4, 9,
- Victor Markowitz5,
- Philip Hugenholtz4, 10,
- Nikos C. Kyrpides4 and
- Hans-Peter Klenk1
- Published: 31 December 2011
Abstract
Desulfurobacterium thermolithotrophum L’Haridon et al. 1998 is the type species of the genus Desulfurobacterium which belongs to the family Desulfurobacteriaceae. The species is of interest because it represents the first thermophilic bacterium that can act as a primary producer in the temperature range of 45–75 °C (optimum 70°C) and is incapable of growing under microaerophilic conditions. Strain BSAT preferentially synthesizes high-melting-point fatty acids (C18 and C20) which is hypothesized to be a strategy to ensure the functionality of the membrane at high growth temperatures. This is the second completed genome sequence of a member of the family Desulfurobacteriaceae and the first sequence from the genus Desulfurobacterium. The 1,541,968 bp long genome harbors 1,543 protein-coding and 51 RNA genes and is a part of the Genomic Encyclopedia of Bacteria and Archaea project.
Keywords
- anaerobic
- thermophilic
- neutrophilic
- obligately chemolithoautotrophic
- Gram-negative
- marine
- sulfur-reducing
- Desulfurobacteriaceae
- GEBA
Introduction
Strain BSAT (= DSM 11699) is the type strain of the species Desulfurobacterium thermolithotrophum, which is the type species of its genus Desulfurobacterium [1], that currently consists of three validly named species [19]. The genus name is derived from the Latin words ‘de’ meaning ‘from’, ‘sulfur’, and ‘bacterium’ meaning ‘a stick, staff’, yielding the Neo-Latin word ‘Desulfurobacterium’ meaning ‘sulfur-reducing rod-shaped bacterium’ [1]. The species epithet is derived from the latinized Greek word ‘thermê’ meaning ‘heat’, the latinized Greek word ‘lithos’ meaning ‘stone’ and the latinized Greek word ‘trophos’ meaning ‘feeder, rearer, one who feeds’, yielding the Neo-Latin word ‘thermolithotrophum’ meaning ‘referring to its thermophilic way of life and lithotrophic metabolism’ [1,2]. Strain BSAT was collected from the Snake Pit vent field on the mid Atlantic Ridge with the help of the submersible Nautile at a depth of 3,500 m [1]. Although it shares most features with other members of the Aquificales, it is distinct in its inability to grow under microaerophilic conditions [1]. Strain BSAT was the first non-hyperthermophilic primary producer isolated from deep-sea vents [1]. Here we present a summary classification and a set of features for D. thermolithotrophum strain BSAT, together with the description of the complete genomic sequencing and annotation.
Classification and features
A representative genomic 16S rRNA sequence of D. thermolithotrophum BSAT was compared using NCBI BLAST [3,4] 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 [5] and the relative frequencies of taxa and keywords (reduced to their stem [6] were determined, weighted by BLAST scores. The most frequently occurring genera were Desulfurobacterium (30.3%), Thermoanaerobacter (18.8%), Thermovibrio (14.2%), Balnearium (11.0%) and Persephonella (4.1%) (80 hits in total). Regarding the two hits to sequences from members of the species, the average identity within HSPs was 98.9%, whereas the average coverage by HSPs was 92.8%. Regarding the single hit to sequences from other members of the genus, the average identity within HSPs was 98.6%, whereas the average coverage by HSPs was 64.4%. Among all other species, the one yielding the highest score was “Desulfurobacterium crinifex” (AJ507320), which corresponded to an identity of 98.6% and HSP coverage of 64.4%. (Note that the Greengenes database uses the INSDC (= EMBL/NCBI/DDBJ) annotation, which is not an authoritative source for nomenclature or classification.) The highest-scoring environmental sequence was AF068800 (‘hydrothermal vent clone VC2.1Bac24’), which showed an identity of 99.7% and an HSP coverage of 92.7%. The most frequently occurring keywords within the labels of all environmental samples which yielded hits were ‘hydrotherm’ (5.4%), ‘vent’ (4.9%), ‘microbi’ (3.6%), ‘water’ (2.9%) and ‘deep’ (2.0%) (167 hits in total). The most frequently occurring keyword within the labels of those environmental samples which yielded hits of a higher score than the highest scoring species was ‘hydrotherm, vent’ (50.0%) (1 hit in total).
Phylogenetic tree highlighting the position of D. thermolithotrophum relative to the type strains of the other species within the order Aquificales. The tree was inferred from 1,422 aligned characters [7,8] of the 16S rRNA gene sequence under the maximum likelihood (ML) criterion [9]. Rooting was done initially using the midpoint method [10] and then checked for its agreement with the current classification (Table 1). The branches are scaled in terms of the expected number of substitutions per site. Numbers adjacent to the branches are support values from 1,000 ML bootstrap replicates [11] (left) and from 1,000 maximum parsimony bootstrap replicates [12] (right) if larger than 60%. Lineages with type strain genome sequencing projects registered in GOLD [13] are labeled with one asterisk, those also listed as ‘Complete and Published’ with two asterisks (referenced in [14–17] and CP002444).
Scanning electron micrograph of D. thermolithotrophum BSAT
Chemotaxonomy
MIGS ID | Property | Term | Evidence code |
---|---|---|---|
Current classification | Domain Bacteria | TAS [20] | |
Phylum ‘Aquificae’ | TAS [22] | ||
Class Aquificae | |||
Order Aquificales | |||
Family Desulfurobacteriaceae | TAS [25] | ||
Genus Desulfurobacterium | |||
Species | Desulfurobacterium thermolithotrophum | TAS [1] | |
MIGS-7 | Strain | BSAT | TAS [1] |
MIGS-12 | Reference for biomaterial | DSM 11699 | TAS [1] |
Gram stain | negative | TAS [1] | |
Cell shape | rod-shaped | TAS [1] | |
Motility | motile | TAS [1] | |
Sporulation | non-sporulating | TAS [1] | |
Temperature range | 40–75°C | TAS [1] | |
Optimum temperature | 70°C | TAS [1] | |
Salinity | 15 to 70 g per l, optimum at 35 g | TAS [1] | |
MIGS-22 | Oxygen requirement | strictly anaerobic | TAS [1] |
Carbon source | CO2 | NAS | |
Energy metabolism | chemolitoautotrophic, sulfur reduction | TAS [1] | |
MIGS-6 | Habitat | marine | TAS [1] |
MIGS-15 | Biotic relationship | free-living | TAS [1] |
Biosafety level | 1 | TAS [28] | |
MIGS-19 | Trophic level | level 1 primary producer | TAS [1] |
MIGS-23.1 | Isolation | deep-sea hydrothermal vent chimney | TAS [1] |
MIGS-4 | Geographic location | Snake Pit vent field, Mid-Atlantic Ridge | TAS [1] |
MIGS-5 | Sample collection time | November/December 1995 | |
MIGS-4.1 | Latitude | 23.36 | |
MIGS-4.2 | Longitude | −44.93 | |
MIGS-4.3 | Depth | 3,500 m | |
MIGS-4.4 | Altitude | −3,500 m | TAS [1] |
Genome sequencing and annotation
Genome project history
Genome sequencing project information
MIGS ID | Property | Term |
---|---|---|
MIGS-31 | Finishing quality | Finished |
MIGS-28 | Libraries used | Four genomic libraries: one 454 pyrosequence standard library, two 454 PE library (10.5 kb insert size), one Illumina library |
MIGS-29 | Sequencing platforms | Illumina GAii, 454 GS FLX Titanium |
MIGS-31.2 | Sequencing coverage | 282.0 × Illumina; 40.0 × pyrosequence |
MIGS-30 | Assemblers | Newbler version 2.3, p Velvet version 0.7.63, phrap version SPS - 4.24 |
MIGS-32 | Gene calling method | Prodigal 1.4, GenePRIMP |
INSDC ID | CP002543 | |
Genbank Date of Release | March 2, 2011 | |
GOLD ID | Gc01671 | |
NCBI project ID | 51497 | |
Database: IMG-GEBA | 2503754020 | |
MIGS-13 | Source material identifier | DSM 11699 |
Project relevance | Tree of Life, GEBA |
Growth conditions and DNA isolation
D. thermolithotrophum strain BSAT, DSM 11699, was grown anaerobically in DSMZ medium 829 (Desulfurobacterium medium) [34] at 70°C. DNA was isolated from 0.5–1 g of cell paste using Qiagen Genomic 500 DNA Kit (Qiagen 10262) following the standard protocol as recommended by the manufacturer without modifications. DNA is available through the DNA Bank Network [35].
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 [36]. Pyrosequencing reads were assembled using the Newbler assembler (Roche). The initial Newbler assembly consisting of 96 contigs in one scaffold was converted into a phrap [37] assembly by making fake reads from the consensus, to collect the read pairs in the 454 paired end library. Illumina GAii sequencing data (45.0 Mb) was assembled with Velvet [38] 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 192.1 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 [37] 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 [36], Dupfinisher [39], or sequencing cloned bridging PCR fragments with subcloning. Gaps between contigs were closed by editing in Consed, by PCR and by Bubble PCR primer walks (J.-F. Chang, unpublished). A total of 101 additional reactions 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 [40]. 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 322.0 × coverage of the genome. The final assembly contained 126,482 pyrosequence and 12,545,740 Illumina reads.
Genome annotation
Genes were identified using Prodigal [41] as part of the Oak Ridge National Laboratory genome annotation pipeline, followed by a round of manual curation using the JGI GenePRIMP pipeline [42]. 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 [33].
Genome properties
Graphical circular map of the genome. From bottom to top: 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) | 1,541,968 | 100.00% |
DNA coding region (bp) | 1,448,295 | 93.93% |
DNA G+C content (bp) | 538,896 | 34.95% |
Number of replicons | 1 | |
Extrachromosomal elements | 0 | |
Total genes | 1,594 | 100.00% |
RNA genes | 51 | 3.20% |
rRNA operons | 2 | |
tRNA genes | 43 | 2.70% |
Protein-coding genes | 1,543 | 96.80% |
Pseudo genes | 34 | 2.13% |
Genes with function prediction | 1,204 | 75.53% |
Genes in paralog clusters | 600 | 37.64% |
Genes assigned to COGs | 1,330 | 83.44% |
Genes assigned Pfam domains | 1,327 | 83.25% |
Genes with signal peptides | 394 | 24.72% |
Genes with transmembrane helices | 322 | 20.20% |
CRISPR repeats | 1 |
Number of genes associated with the general COG functional categories
Code | value | %age | Description |
---|---|---|---|
J | 142 | 9.7 | Translation, ribosomal structure and biogenesis |
A | 0 | 0.0 | RNA processing and modification |
K | 47 | 3.2 | Transcription |
L | 126 | 8.6 | Replication, recombination and repair |
B | 1 | 0.1 | Chromatin structure and dynamics |
D | 20 | 1.4 | Cell cycle control, cell division, chromosome partitioning |
Y | 0 | 0.0 | Nuclear structure |
V | 13 | 0.9 | Defense mechanisms |
T | 52 | 3.6 | Signal transduction mechanisms |
M | 110 | 7.5 | Cell wall/membrane/envelope biogenesis |
N | 67 | 4.6 | Cell motility |
Z | 0 | 0.0 | Cytoskeleton |
W | 0 | 0.0 | Extracellular structures |
U | 74 | 5.1 | Intracellular trafficking, secretion, and vesicular transport |
O | 55 | 3.8 | Posttranslational modification, protein turnover, chaperones |
C | 113 | 7.7 | Energy production and conversion |
G | 42 | 2.9 | Carbohydrate transport and metabolism |
E | 108 | 7.4 | Amino acid transport and metabolism |
F | 57 | 3.9 | Nucleotide transport and metabolism |
H | 88 | 6.0 | Coenzyme transport and metabolism |
I | 38 | 2.6 | Lipid transport and metabolism |
P | 57 | 3.9 | Inorganic ion transport and metabolism |
Q | 13 | 0.9 | Secondary metabolites biosynthesis, transport and catabolism |
R | 140 | 9.6 | General function prediction only |
S | 97 | 6.6 | Function unknown |
- | 264 | 16.6 | Not in COGs |
Declarations
Acknowledgements
We would like to gratefully acknowledge the help of Thomas Hader (University of Regensburg) for growing D. thermolithotrophum cultures. This work was performed under the auspices of the US Department of Energy’s 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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