- Open Access
Complete genome sequence of Hydrogenobacter thermophilus type strain (TK-6T)
- Ahmet Zeytun1, 3,
- Johannes Sikorski2,
- Matt Nolan1,
- Alla Lapidus1,
- Susan Lucas1,
- James Han1,
- Hope Tice1,
- Jan-Fang Cheng1,
- Roxanne Tapia1, 3,
- Lynne Goodwin1, 3,
- Sam Pitluck1,
- Konstantinos Liolios1,
- Natalia Ivanova1,
- Konstantinos Mavromatis1,
- Natalia Mikhailova1,
- Galina Ovchinnikova1,
- Amrita Pati1,
- Amy Chen4,
- Krishna Palaniappan4,
- Olivier D. Ngatchou-Djao5,
- Miriam Land1, 6,
- Loren Hauser1, 6,
- Cynthia D. Jeffries1, 6,
- Cliff Han1, 3,
- John C. Detter1, 3,
- Susanne Übler7,
- Manfred Rohde5,
- Brian J. Tindall2,
- Markus Göker2,
- Reinhard Wirth7,
- Tanja Woyke1,
- James Bristow1,
- Jonathan A. Eisen1, 8,
- Victor Markowitz4,
- Philip Hugenholtz1, 9,
- Hans-Peter Klenk2 and
- Nikos C. Kyrpides1
- Published: 29 April 2011
Abstract
Hydrogenobacter thermophilus Kawasumi et al. 1984 is the type species of the genus Hydrogenobacter. H. thermophilus was the first obligate autotrophic organism reported among aerobic hydrogen-oxidizing bacteria. Strain TK-6T is of interest because of the unusually efficient hydrogen-oxidizing ability of this strain, which results in a faster generation time compared to other autotrophs. It is also able to grow anaerobically using nitrate as an electron acceptor when molecular hydrogen is used as the energy source, and able to aerobically fix CO2via the reductive tricarboxylic acid cycle. This is the fifth completed genome sequence in the family Aquificaceae, and the second genome sequence determined from a strain derived from the original isolate. Here we describe the features of this organism, together with the complete genome sequence and annotation. The 1,742,932 bp long genome with its 1,899 protein-coding and 49 RNA genes is a part of the Genomic Encyclopedia of Bacteria and Archaea project.
Keywords
- strictly thermophilic
- obligately chemolithoautotrophic
- Gram-negative
- aerobic
- hydrogen-oxidizing
- nonmotile
- non sporeforming
- rod shaped
- Aquificaceae
- Aquificae
- GEBA
Introduction
Strain TK-6T (= DSM 6534 = JCM 7687 = NBRC 102181) is the type strain of Hydrogenobacter thermophilus, which in turn is the type species of the genus Hydrogenobacter [1]. Currently, there are four validly published species in the genus Hydrogenobacter, one of which has subsequently been reclassified as Hydrogenobaculum acidophilum. Strain TK-6T was previously isolated by Kawasumi in 1980 [2]. The genus name Calderobacterium Kryukov et al. 1984 is, based on page priority, a later heterotypic synonym of Hydrogenobacter Kawasumi et al. 1984 [3], because of similar genetic, phenotypic and biochemical properties between the type strains of H. thermophilus and Calderobacterium hydrogenophilum. Despite the relatively high degree of 16S rRNA gene sequence similarity between the two species, DNA-DNA hybridization [4] indicates that they may be considered to be different species within the genus Hydrogenobacter [3]. The genus name Hydrogenobacter is derived from the Latin words hydrogenum, meaning ‘that which produces water’ and bacter, referring to a rod that forms water when exposed to oxygen. The species epithet thermophilus derives from the Greek words therme, heat, and philus, loving, meaning a heat-loving organism. Strain TK-6T was isolated from hot springs located on the Izu peninsula in Japan [1]. Some strains of H. thermophilus were also isolated from a geothermal spring in Tuscany, Italy [5,6]. Other strains similar to H. thermophilus have been isolated from different environments, including a saline hot spring in Japan for ‘H. halophilus’ [7], and a volcanic area in Iceland for Hydrogenobacter strain H-1 [8], strains T3, T13 and T171 [5]. Until 1985, H. thermophilus was the only obligate autotroph among all aerobic hydrogen-oxidizing bacteria reported so far [9,10]. The activities of enzymes such as NADH:ferredoxin reductase (EC 1.18.1.3) and NAD-reducing hydrogenase (EC 1.12.1.2) were studied extensively in strain TK-6T [11]. Another genome sequence of a strain derived from the original isolate, presumably held in the lab of one of the co-authors, has been published recently without much metadata [12]. Here we present a summary classification and a set of features for H. thermophilus strain TK-6T, together with the description of the complete genomic sequencing and annotation.
Classification and features
The 16S rRNA gene sequence of the strain TK-6T (Z30214) shows the highest degree of sequence identity, 97%, to the type strain of H. hydrogenophilus [6]. Further analysis shows 96% 16S rRNA gene sequence identity with an uncultured Aquificales bacterium clone pKA (AF453505) from a near-neutral thermal spring in Kamchatka, Russia. The single genomic 16S rRNA sequence of H. thermophilus was compared with the most recent release of the Greengenes database [13] using NCBI BLAST under default values and the relative frequencies of taxa and keywords, weighted by BLAST scores, were determined. The five most frequent genera were Hydrogenobacter (52.4%), Thermocrinis (18.8%), Aquifex (10.3%), Sulfurihydrogenibium (6.2%) and Hydrogenivirga (5.7%). Regarding hits to sequences from other members of the genus, the average identity within HSPs (high-scoring segment pairs) was 96.1%, whereas the average coverage by HSPs was 93.5%. The species yielding the highest score was H. hydrogenophilus. The five most frequent keywords within the labels of environmental samples which yielded hits were ‘hot’ (6.5%), ‘yellowstone’ (5.8%), ‘spring’ (5.6%), ‘national/park’ (5.4%) and ‘microbial’ (3.9%). These keywords corroborate what is known from the ecology and physiology of strain TK-6T [1,2]. The two most frequent keywords within the labels of environmental samples which yielded hits of a higher score than the highest scoring species were ‘aquificales’ (34.1%) and ‘hot/spring’ (32.9%).
Phylogenetic tree highlighting the position of H. thermophilus TK-6T relative to the type strains of the other species within the genus and to the type strains of the other genera within the family Aquificaceae. The trees were inferred from 1,423 aligned characters [14,15] of the 16S rRNA gene sequence under the maximum likelihood criterion [16] and rooted in accordance with the current taxonomy [17]. The branches are scaled in terms of the expected number of substitutions per site. Numbers above branches are support values from 1,000 bootstrap replicates [18] if larger than 60%. Lineages with type strain genome sequencing projects registered in GOLD [19] are shown in blue, published genomes in bold [12,20,21].
Scanning electron micrograph of H. thermophilus TK-6T
Classification and general features of H. thermophilus TK-6T according to the MIGS recommendations [22]
MIGS ID | Property | Term | Evidence code |
---|---|---|---|
Current classification | Domain Bacteria | TAS [23] | |
Phylum Aquificae | |||
Class Aquificae | |||
Order Aquificales | |||
FamilyAquificaceae | |||
Genus Hydrogenobacter | TAS [1] | ||
Species Hydrogenobacter thermophilus | TAS [1] | ||
Type strain TK-6 | TAS [1] | ||
Gram stain | negative | TAS [1] | |
Cell shape | straight rods | TAS [1] | |
Motility | non-motile | TAS [1] | |
Sporulation | no | TAS [1] | |
Temperature range | 50°C–78°C | TAS [30] | |
Optimum temperature | 70°C–75°C | TAS [1] | |
Salinity | not reported | NAS | |
MIGS-22 | Oxygen requirement | aerobic | TAS [1] |
Carbon source | CO2 | TAS [1] | |
Energy source | H2, thiosulfate, obligate chemolithoautotrophic | TAS [1] | |
MIGS-6 | Habitat | soil near hot spring | TAS [1] |
MIGS-15 | Biotic relationship | free living | NAS |
MIGS-14 | Pathogenicity | not reported | NAS |
Biosafety level | 1 | TAS [31] | |
Isolation | hot spring | TAS [1] | |
MIGS-4 | Geographic location | Izu peninsula, Japan | |
MIGS-5 | Sample collection time | 1980 or before | |
MIGS-4.1 | Latitude | approx. 34.9 | NAS |
MIGS-4.2 | Longitude | 138.9 | |
MIGS-4.3 | Depth | not reported | |
MIGS-4.4 | Altitude | not reported |
Chemotaxonomy
The major cellular fatty acids found in strain TK-6T were C18:0 and C20:1 [1,47]. These two fatty acids comprised about 80% of the total cellular fatty acids [1,47]. The minor components detected were C16:0, C16:1 and C18:1. C14:0 acids (indicative of the presence of a lipopolysaccharide) and a C21:0 cyclopropane acid, representing less than 10% of the total cellular fatty acids [1,47]. The detailed fatty acid composition of the strain TK-6T is available in [27] and [47]. The main respiratory lipoquinone is an unusual sulfur-containing quinone, a 2-methylthio-3-VI, VII-tetrahydroheptaprenyl-1,4-naphthoquinone (i.e., methionaquinone 7, MTK-7) [48,49]. Strain TK-6T contains glycerol-ether basedlipids, as well as acyl glycerides [47]. It should be noted that the ether lipids are not of the type found in members of the Archaea, since the side chains are alkyl straight chain and not isoprenoid. The presence of glycerol monoethers (GME) (1.2 µ mol/g dwt) is a characteristic feature of the strain TK-6T, the main one being GME-18:0 (82.7% wt) [27,47]. GME-20:1 (11.1% wt), GME-20:0 (3.5 wt), and GME-18:1 (2.7% wt) were also detected in strain TK-6T [27,47]. No glycerol diether (GDE) was detected [27,47].
Investigations of the polar lipids have shown that they comprise phosphatidylglycerol, phosphatidylinositol, phosphatidylaminopentantetrol and a small amount of an unidentified phospholipid. The sum of these chemotaxomonic features appears to be characteristic of members of the genus Hydrogenobacter, with features such as the presence of methionaquinone, a polar lipid pattern containing phosphatidylglycerol, phosphatidylinositol and phosphatidylaminopentantetrol and the presence of C18:0 and C20:1 fatty acids being taxonomic and evolutionary markers for at least members of the genera Hydrogenobacter, Hydrogenobaculum, Aquifex and Thermoncrinis. This has been discussed in a previous SIGS paper [50].
Genome sequencing and annotation
Genome project history
Genome sequencing project information
MIGS ID | Property | Term |
---|---|---|
MIGS-31 | Finishing quality | Finished |
MIGS-28 | Libraries used | One 454 pyrosequence standard library, one 454 PE (20kb insert size) and one Illumina standard library |
MIGS-29 | Sequencing platforms | 454 GS FLX Titanium, Illumina GAii |
MIGS-31.2 | Sequencing coverage | 82.1× pyrosequence, 264.4 × Illumina |
MIGS-30 | Assemblers | Newbler version 2.3-PreRelease-10-21-2009-gcc-4.1.2, phrap |
MIGS-32 | Gene calling method | Prodigal 1.4, GenePRIMP |
INSDC ID | CP002221 | |
Genbank Date of Release | October 15, 2010 | |
GOLD ID | Gc01411 | |
NCBI project ID | 41547 | |
Database: IMG-GEBA | 2502957034 | |
MIGS-13 | Source material identifier | DSM 6534 |
Project relevance | Tree of Life, GEBA |
Growth conditions and DNA isolation
H. thermophilus TK-6T, DSM 6534, was grown in DSMZ medium 533 (Thermophilic hydrogen bacteria medium) [53] with 5% oxygen at 72°C. DNA was isolated from 0.5–1 g of cell paste using Qiagen Genomic 500 DNA Kit (Qiagen, Hilden, Germany) following the standard protocol as recommended by the manufacturer. DNA is available through the DNA Bank Network [54].
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 [55]. Pyrosequencing reads were assembled using the Newbler assembler version 2.3-PreRelease-10-21-2009-gcc-4.1.2-threads (Roche). The initial Newbler assembly consisted of 19 contigs in one scaffold which was converted into a phrap assembly by making fake reads from the consensus, collecting the read pairs in the 454 paired end library. Illumina GAii sequencing data (449.5 Mb) was assembled with Velvet [56] 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 143.2 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 [57] 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 [55], Dupfinisher, or sequencing cloned bridging PCR fragments with subcloning or transposon bombing (Epicentre Biotechnologies, Madison, WI) [58]. Gaps between contigs were closed by editing in Consed, by PCR and by Bubble PCR primer walks (J.-F.Chang, unpublished). A total of 24 additional Sanger 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 [59]. 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 346.5 × coverage of the genome. Final assembly contains 454,097 pyrosequence and 12,484,847 Illumina reads.
Genome annotation
Genes were identified using Prodigal [60] as part of the Oak Ridge National Laboratory genome annotation pipeline, followed by a round of manual curation using the JGI GenePRIMP pipeline [61]. The predicted CDSs were translated and used to search the National Center for Biotechnology Information (NCBI) nonredundant database, UniProt, TIGRFam, 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 [62].
Genome properties
Graphical circular map of the genome. 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) | 1,742,932 | 100.00% |
DNA coding region (bp) | 1,666,175 | 95.60% |
DNA G+C content (bp) | 766,905 | 44.00% |
Number of replicons | 1 | |
Extrachromosomal elements | 0 | |
Total genes | 1,948 | 100.00% |
RNA genes | 49 | 2.52% |
rRNA operons | 1 | |
Protein-coding genes | 1,899 | 97.48% |
Pseudo genes | 30 | 1.54% |
Genes with function prediction | 1,361 | 69.87% |
Genes in paralog clusters | 183 | 9.39% |
Genes assigned to COGs | 1,441 | 73.97% |
Genes assigned Pfam domains | 1,501 | 77.05% |
Genes with signal peptides | 287 | 14.73% |
Genes with transmembrane helices | 381 | 19.56% |
CRISPR repeats | 1 |
Number of genes associated with the general COG functional categories
Code | value | %age | Description |
---|---|---|---|
J | 134 | 8.6 | Translation, ribosomal structure and biogenesis |
A | 0 | 0.0 | RNA processing and modification |
K | 52 | 3.3 | Transcription |
L | 85 | 5.4 | Replication, recombination and repair |
B | 2 | 0.1 | Chromatin structure and dynamics |
D | 19 | 1.3 | Cell cycle control, cell division, chromosome partitioning |
Y | 0 | 0.0 | Nuclear structure |
V | 21 | 1.3 | Defense mechanisms |
T | 53 | 3.4 | Signal transduction mechanisms |
M | 128 | 8.2 | Cell wall/membrane/envelope biogenesis |
N | 23 | 1.5 | Cell motility |
Z | 1 | 0.0 | Cytoskeleton |
W | 0 | 0.0 | Extracellular structures |
U | 56 | 3.6 | Intracellular trafficking and secretion, and vesicular transport |
O | 74 | 4.7 | Posttranslational modification, protein turnover, chaperones |
C | 182 | 11.6 | Energy production and conversion |
G | 58 | 3.7 | Carbohydrate transport and metabolism |
E | 118 | 7.5 | Amino acid transport and metabolism |
F | 52 | 3.3 | Nucleotide transport and metabolism |
H | 107 | 6.8 | Coenzyme transport and metabolism |
I | 43 | 2.7 | Lipid transport and metabolism |
P | 78 | 5.0 | Inorganic ion transport and metabolism |
Q | 15 | 1.0 | Secondary metabolites biosynthesis, transport and catabolism |
R | 167 | 10.7 | General function prediction only |
S | 100 | 6.4 | Function unknown |
- | 507 | 26.3 | Not in COGs |
Insights into the genome
While the sequencing of the genome described in this paper was underway, Arai et al. from University of Tokyo published the first version of the H. thermophilus TK-6T genome [19, AP011112]. We take the opportunity to compare the two completed genome sequences, because the history of the two strains designated TK-6T might differ since the original isolation of the strain by Kawasumu et al. [1], more than a 25 years ago. The first of the two genomes was published by a team of researchers located at the same place where the strain was originally analyzed, with Yasuo Igarashi participating in both, the original description of the strain and the genome analysis. According to personal information by Dr. Arai Hiroyuki (lead author in [19]), the genome was sequenced from clone and fosmid libraries generated by a strain subcultured in the lab since the time of the initial isolation. A fresh culture of the strain from JCM was used for final gap filling and error checking. The DSM 6534 version of the genome was generated from cryopreserved material, which DSMZ received in 1991 from Tohru Kodama of University of Tokyo, and the strain was preserved by storage in liquid nitrogen since it was accessed.
Comparison of Genome Statistics
Attribute | DSM 6534 | U of Tokyo | difference |
---|---|---|---|
Genome size (bp) | 1,742,932 | 1,744,135 | +1,203 |
DNA coding region (bp) | 1,666,175 | 1,669,712 | +3,537 |
DNA G+C content (bp) | 766,905 | 766,984 | +79 |
Number of replicons | 1 | 1 | 1 |
Extrachromosomal elements | 0 | 0 | 0 |
Total genes | 1,948 | 1,941 | −7 |
RNA genes | 49 | 48 | −1 |
rRNA operons | 1 | 1 | 1 |
Protein-coding genes | 1,899 | 1,893 | −6 |
Pseudo genes | 30 | 0 | −30 |
Genes with function prediction | 1,361 | 1,349 | −12 |
Genes in paralog clusters | 183 | 175 | −8 |
Genes assigned to COGs | 1,441 | 1,430 | −11 |
Genes assigned Pfam domains | 1,501 | 1,489 | −12 |
Genes with signal peptides | 287 | 528 | +241 |
Genes with transmembrane helices | 381 | 385 | +4 |
CRISPR repeats | 1 | 2 | +1 |
The Japanese strain has 1,868 (out of 1,893) protein coding genes identical to the DSMZ strain which is 98.7% of the genome. This means there are 25 genes in the Japanese strain that are not in the DSMZ strain, all except L34P are hypothetical genes. L34P is however present in the version of the genome as presented in this paper, but was missed from the ORF calling/annotation. We also identified 24 genes in the genome sequenced from the DSMZ strain that were missing in the Arai et al. strain. Also most of these were again hypothetical genes. The abundance profiles for both genomes were almost identical, with glycosyltransferase (COG0438) being the most frequent gene in both versions (eleven copies), followed by seven copies of an outer membrane protein (COG1538), each. The DSM 6534 genome contains seven copies of transposase IS605 OrfB (COG0675), whereas Tokyo contains five copies of it.
The DSM 6534 version of the genome also contains more copies of cation transport ATPase (COG0474, 4 vs. 2), nitrogenase molybdenum-iron protein, alpha and beta chains (COG2710, 4 vs. 2), acetyl/propionyl-CoA carboxylase, alpha subunit (COG4779, 4 vs. 3), Fe-S oxidoreductases (GCO0474, 3 vs. 2), catabolite gene activator and regulatory subunit of cAMP-dependent protein kinases (COG0664, 3 vs. 2), cation transport ATPase (COG2217, 3 vs. 2), DNA modification methylase (COG0862, 2 vs. 1), hemolysins and related proteins containing CBS domains (COG1253, 2 vs. 1). Phosphoketolase (COG3957), an uncharacterized MobA-related protein (COG2068) and an uncharacterized conserved protein (COG4121) were identified in one copy, each, in the DSM 6534 genome, but absent in the U Tokyo version. The U Tokyo version contains more copies of selenocysteine-containing anaerobic dehydrogenases, (COG0243, 5 vs. 1), as well as,1-acyl-sn-glycerol-3-phosphate acyltransferase (COG02043) and K+-transporting ATPase, A chain (COG2060, 2 vs. 1, each)
Declarations
Acknowledgements
We would like to gratefully acknowledge the help of Susanne Schneider (DSMZ) for DNA extraction and quality analysis. 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 599/1-1.
Authors’ Affiliations
References
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