Open Access

Complete genome sequence of Oceanithermus profundus type strain (506T)

  • Amrita Pati
  • , Xiaojing Zhang
  • , Alla Lapidus
  • , Matt Nolan
  • , Susan Lucas
  • , Tijana Glavina Del Rio
  • , Hope Tice
  • , Jan-Fang Cheng
  • , Roxane Tapia,
  • , Cliff Han,
  • , Lynne Goodwin,
  • , Sam Pitluck
  • , Konstantinos Liolios
  • , Ioanna Pagani
  • , Natalia Ivanova
  • , Konstantinos Mavromatis
  • , Amy Chen
  • , Krishna Palaniappan
  • , Loren Hauser,
  • , Cynthia D. Jeffries,
  • , Evelyne-Marie Brambilla
  • , Alina Röhl
  • , Romano Mwirichia
  • , Manfred Rohde
  • , Brian J. Tindall
  • , Johannes Sikorski
  • , Reinhard Wirth
  • , Markus Göker
  • , Tanja Woyke
  • , John C. Detter,
  • , James Bristow
  • , Jonathan A. Eisen,
  • , Victor Markowitz
  • , Philip Hugenholtz,
  • , Nikos C. Kyrpides
  • , Hans-Peter Klenk
  • and Miriam Land,
Corresponding author

DOI: 10.4056/sigs.1734292

Received: 29 April 2011

Published: 29 April 2011

Abstract

Oceanithermus profundus Miroshnichenko et al. 2003 is the type species of the genus Oceanithermus, which belongs to the family Thermaceae. The genus currently comprises two species whose members are thermophilic and are able to reduce sulfur compounds and nitrite. The organism is adapted to the salinity of sea water, is able to utilize a broad range of carbohydrates, some proteinaceous substrates, organic acids and alcohols. This is the first completed genome sequence of a member of the genus Oceanithermus and the fourth sequence from the family Thermaceae. The 2,439,291 bp long genome with its 2,391 protein-coding and 54 RNA genes consists of one chromosome and a 135,351 bp long plasmid, and is a part of the Genomic Encyclopedia of Bacteria and Archaea project.

Keywords:

microaerophilicnon-motileGram-negativenitrate-reducingmoderate thermophilicneutrophilicchemolithoheterotrophichydrothermal ventThermaceaeGEBA

Introduction

Strain 506T (DSM 14977 = NBRC 100410 = VKM B-2274) is the type strain of Oceanithermus profundus, which is the type species of the genus Oceanithermus [1] of the family Thermaceae [2]. Together with O. desulfurans, there are currently two species placed in the genus [1,3]. The generic name derives from the Latin noun oceanus, meaning ocean and the Neo-Latin masc. substantive (from Gr. adj. thermos) thermus which means hot. Therefore, the name Oceanithermus refers to warmth-loving organisms living in the ocean. The species epithet is derived from the Latin adjective profundus meaning deep, which means pertaining to the abyss, pertaining to the depths of the ocean [1]. Strain 506T was first isolated from samples of hydrothermal fluids and chimneys collected at the 13ºN hydrothermal vent field on the East Pacific Rise at a depth of 2600 m [1]. There are no further cultivated strains of this species known. The other member of the genus, O. desulfurans, is a thermophilic, sulfur-reducing bacterium isolated from a sulfide chimney in Suiyo Seamount, in the Western Pacific [3]. Here we present a summary classification and a set of features for O. profundus 506T, together with the description of the complete genomic sequencing and annotation.

Classification and features

A representative genomic 16S rRNA sequence of strain 506T 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 [4] and the relative frequencies, weighted by BLAST scores, of taxa and keywords (reduced to their stem) [5] were determined. The five most frequent genera were Thermus (52.0%), Meiothermus (37.0%), Oceanithermus (7.6%), Marinithermus (2.0%) and Vulcanithermus (1.4%) (156 hits in total). Regarding the four hits to sequences from members of the species, the average identity within HSPs was 99.6%, whereas the average coverage by HSPs was 94.8%. Regarding the two hits to sequences from other members of the genus, the average identity within HSPs was 99.3%, whereas the average coverage by HSPs was 91.0%. Among all other species, the one yielding the highest score was O. desulfurans, which corresponded to an identity of 99.3% and an HSP coverage of 91.0%. The highest-scoring environmental sequence was EU555123 ('Microbial Sulfide Hydrothermal Vent Field Juan de Fuca Ridge Dudley hydrothermal vent clone 4132B16'), which showed an identity of 99.1% and an HSP coverage of 98.0%. The five most frequent keywords within the labels of environmental samples which yielded hits were 'spring' (8.2%), 'hot' (6.2%), 'microbi' (4.5%), 'geochem, nation, park, yellowston' (2.8%) and 'hydrotherm/vent' (2.5%) (94 hits in total). The five most frequent keywords within the labels of environmental samples which yielded hits of a higher score than the highest scoring species were 'hydrotherm/vent' (12.2%), 'field, microbi, ridg' (6.1%), 'fluid' (5.9%), 'dudlei, fuca, juan, sulfid' (3.1%) and 'degre, east, north, ocean, pacif, rise' (3.0%) (3 hits in total). These 16S BLAST results are a confirmation of the kind of environment from which the living strain was isolated and therefore fits the description of the isolate.

Figure 1 shows the phylogenetic neighborhood of O. profundus in a 16S rRNA based tree. The sequences of the two identical 16S rRNA gene copies in the genome differ by one nucleotide from the previously published 16S rRNA sequence (AJ430586).

Figure 1

Phylogenetic tree highlighting the position of O. profundus relative to the other type strains within the family Thermaceae. The tree was inferred from 1,420 aligned characters [6,7] of the 16S rRNA gene sequence under the maximum likelihood criterion [8]. Rooting was initially done using the midpoint method [9] and then checked for its accordance with the current taxonomy (see Table 1) and rooted accordingly. The branches are scaled in terms of the expected number of substitutions per site. Numbers to the right of bifurcations are support values from 1,000 bootstrap replicates [10] if larger than 60%. Lineages with type strain genome sequencing projects that are registered in GOLD [11] but remain unpublished are labeled with one asterisk, published genomes with two asterisks [12-14].

The cells of O. profundus are described as non-motile, rod-shaped, 0.5 – 0.7 µm in diameter and of various lengths (Figure 2). When grown on proteinaceous substrates, old cultures of O. profundus form filaments and large spheres resembling the ‘rotund bodies’ typical of aged cells of Thermus species [1,15]. The organism is Gram-negative and non spore-forming (Table 1).

Figure 2

Scanning electron micrograph of O. profundus 506T

Table 1

Classification and general features of O. profundus 506T according to the MIGS recommendations [16].

MIGS ID

    Property

    Term

   Evidence code

    Current classification

    Domain Bacteria

   TAS [17]

    Phylum “Deinococcus-Thermus

   TAS [18,19]

    Class Deinococci

   TAS [20,21]

    Order Thermales

   TAS [21,22]

    Family Thermaceae

   TAS [21,23]

    Genus Oceanithermus

   TAS [1]

    Species Oceanithermus profundus

   TAS [1]

    Type strain 506

   TAS [1]

    Gram stain

    negative

   TAS [1]

    Cell shape

    rod-shaped

   TAS [1]

    Motility

    non-motile

   TAS [1]

    Sporulation

    none

   TAS [1]

    Temperature range

    40-68ºC

   TAS [1]

    Optimum temperature

    60°C

   TAS [1]

    Salinity

    1%-5%, optimum 3% NaCl

   TAS [1]

MIGS-22

    Oxygen requirement

    microaerophile

   TAS [1]

    Carbon source

    carbohydrates

   TAS [1]

    Energy metabolism

    chemoorganoheterotroph, lithoheterotroph, organotroph

   TAS [1]

MIGS-6

    Habitat

    deep sea, hydrothermal vent, marine

   TAS [1]

MIGS-15

    Biotic relationship

    free-living

   TAS [1]

MIGS-14

    Pathogenicity

    none

   NAS

    Biosafety level

    1

   NAS [24]

    Isolation

    deep-sea hot vent

   TAS [1]

MIGS-4

    Geographic location

    East Pacific Rise

   TAS [1]

MIGS-5

    Sample collection time

    1999

   TAS [1]

MIGS-4.1

    Latitude

    12.8

   TAS [1]

MIGS-4.2

    Longitude

    103.93

   TAS [1]

MIGS-4.3

    Depth

    2,600 m

   TAS [1]

MIGS-4.4

    Altitude

    -2,600 m

   NAS

Evidence codes - IDA: Inferred from Direct Assay (first time in publication); TAS: Traceable Author Statement (i.e., a direct report exists in the literature); NAS: Non-traceable Author Statement (i.e., not directly observed for the living, isolated sample, but based on a generally accepted property for the species, or anecdotal evidence). These evidence codes are from of the Gene Ontology project [25] If the evidence code is IDA, then the property was directly observed by one of the authors or an expert mentioned in the acknowledgements.

O. profundus is microaerophilic, only being able to grow at oxygen concentrations below 6% [1]. No growth has been observed in an atmosphere of air, either in liquid medium or on plates. In an agar tube containing 5 ml of basal medium supplemented with 2 g sucrose and 1 g tryptone per liter with air in the headspace (10 ml), growth occurs in a zone located 20 mm below the agar/air interface [1]. Alternatively, the organism grows anaerobically using nitrate as the electron acceptor. O. profundus grows within a temperature range of 40-68ºC, optimal growth being observed at 60ºC. At 60ºC, it grows between pH 5.5 and 8.4, with an optimum around 7.5 [1]. Strain 506T grows at NaCl concentrations ranging from 10 to 50 g/l, with an optimum at 30 g/1 [1]. The organism is oxidase- and catalase positive and is able to utilize a wide spectrum of carbohydrates in the presence of either nitrate or oxygen [1]. The highest cell yield is observed in the presence of nitrate with fructose, maltose, sucrose, trehalose, galactose, rhamnose or xylose. Glucose, lactose and starch are utilized, but no growth has been reported with ribose, galactose, arabinose, dextrin or cellobiose [1]. Acetate and propionate are produced during growth with sucrose as a growth substrate and nitrate as the electron acceptor. Nitrite is the only product of denitrification [1]. O. profundus grows well with complex proteinaceous substrates such as beef extract, tryptone or papaic digest of soybean (1-1.5 g/l). However, growth is strongly inhibited by higher concentrations of these substrates [1]. The isolate does not grow with Casamino acids or yeast extract as sole sources of carbon and energy, though 100 mg/l yeast extract is required for growth [1]. O. profundus is able to utilize acetate, pyruvate and propionate as growth substrates. It also grows with methanol, ethanol and mannitol, though the cell yield is lower [1]. O. profundus is able to grow lithoheterotrophically using molecular hydrogen as the energy source, yeast extract as the carbon source and nitrate as the electron acceptor. Other electron acceptors (sulfate, elemental sulfur, thiosulfate and nitrite) do not support growth, regardless of growth substrate [1]. Detailed studies on the metabolism of maltose, acetate, pyruvate, and hydrogen have been undertaken by Fedosov et al. [26].

Chemotaxonomy

The polar lipid pattern of strain 506T comprises three phospholipids, whereas glycolipids have not been detected [1]. This differentiates the organism from members of the genera Vulcanithermus, Rhabdothermus, Thermus and Meiothermus, where phospholipids and glycolipids have both been detected [27,28]. It should be noted that the major phospholipid detected in O. profundus has the same Rf and staining behavior as the 2′-O-(1, 2-diacyl-sn-glycero-3-phospho)–3′-O-(α-N-acetyl-glucosaminyl)-N-glyceroyl alkylamine reported to occur in members of the genera Meiothermus and Thermus [29]. On the basis of Rf value and staining behavior this lipid also appears to be present in members of the genera Vulcanithermus and Rhabdothermus, which also synthesize glycolipids [30,31]. Although members of the genus Deinococcus may also produce glycolipids in addition to a novel series of phosphoglycolipids [32,33] the latter are absent in members of the genera Thermus and Meiothermus. The absence of glycolipids was one of the arguments for Miroshnichenko et al. for placing strain 506T in a new genus [1].

Menaquinones are the sole respiratory lipoquinones detected, with MK-8 predominating (95%) and MK-9 being present in smaller proportions (5%) [1]. The predominance of MK-8 is consistent with reports of MK-8 in members of the genera Thermus, Meiothermus [34,35], Marinithermus [36] Vulcanithermus, Rhabdothermus, Truepera, Deinobacterium and Deinococcus [30-33,37]. However, the presence of MK-9, albeit at only 5%, appears to be a unique feature of O. profundus.

The fatty acids comprise mainly iso- and anteiso-branched fatty acids though iso-unsaturated fatty acids are also present [1]. The major fatty acids are iso-C15:1ω7 (7.7%), iso-C15:0 (33.2%), iso-C16:1ω8 (2.6 iso-C16:0 (3.3%), iso-C17:1ω7c (18.8%), iso-C17:0 (12.3%), anteiso-C15:0 (5.1%) and anteiso-C17:0 (5.4%) [1]. The presence of iso- and anteiso-branched fatty acids is a feature of members of the genera Deinococcus, Thermus, Meiothermus, Vulcanithermus, Rhabdothermus and Marinithermus [27,28,30-34,37]. The presence of unsaturated branched-chain fatty acids is a distinctive feature of members of the genera Oceanithermus, Vulcanithermus and Rhabdothermus within the family Thermaceae. The unsaturated fatty acid content of the isolate is also higher (33-37%) as compared to the closest relative O. desulfurans (18%) [3].

Genome sequencing and annotation

Genome project history

This organism was selected for sequencing on the basis of its phylogenetic position [38] and is part of the Genomic Encyclopedia of Bacteria and Archaea project [39]. The genome project is deposited in the Genome On Line Database [11] and the complete genome sequence is deposited in GenBank. Sequencing, finishing and annotation were performed by the DOE Joint Genome Institute (JGI). A summary of the project information is shown in Table 2.

Table 2

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 (17 kb insert size), one Illumina library

MIGS-29

   Sequencing platforms

    Illumina GAii, 454 GS FLX Titanium

MIGS-31.2

   Sequencing coverage

    85.5 × Illumina; 197.3 × pyrosequence

MIGS-30

   Assemblers

    Newbler version 2.3-PreRelease-8-23-2009, Velvet, phrap

MIGS-32

   Gene calling method

    Prodigal 1.4, GenePRIMP

   INSDC ID

    CP002361 chromosome    CP002362 plasmid OCEPR01

   Genbank Date of Release

    December 7, 2010

   GOLD ID

    Gc01553

   NCBI project ID

    40223

   Database: IMG-GEBA

    2503508010

MIGS-13

   Source material identifier

    DSM 14977

   Project relevance

    Tree of Life, GEBA

Growth conditions and DNA isolation

O. profundus strain 506T, DSM 14977, was grown anaerobically in DSMZ medium 975 (Oceanithermus profundus medium) [40] at 60°C. DNA was isolated from 0.5-1 g of cell paste using Jetflex Genomic DNA Purification Kit following the standard protocol as recommended by the manufacturer, but with an additional proteinase K (20 µl) digestion for 45 min at 58°C. DNA is available through the DNA Bank Network [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 2.3-PreRelease-8-23-2009 (Roche). The initial Newbler assembly, consisting of nine contigs in four scaffolds, was converted into a phrap assembly by [43] making fake reads from the consensus, to collect the read pairs in the 454 paired end library. Illumina GAii sequencing data (208 Mb) 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 306.1 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 [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, or sequencing cloned bridging PCR fragments with subcloning or transposon bombing (Epicentre Biotechnologies, Madison, WI) [45]. Gaps between contigs were closed by editing in Consed, by PCR and by Bubble PCR primer walks (J.-F.Chang, unpublished). A total of 177 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 [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 282.8 × coverage of the genome. The final assembly contained 1,258,374 pyrosequence and 5,792,221 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) [49].

Genome properties

The genome consists of a 2,303,940 bp long chromosome with a G+C content of 70% and a 135,351 bp plasmid with a G+C content of 66% (Table 3 and Figure 3). Of the 2,445 genes predicted, 2,391 were protein-coding genes, and 54 RNAs; 18 pseudogenes were also identified. The majority of the protein-coding genes (69.9%) were assigned with a putative function while the remaining ones were annotated as hypothetical proteins. The distribution of genes into COGs functional categories is presented in Table 4.

Table 3

Genome Statistics

Attribute

   Value

  % of Total

Genome size (bp)

   2,439,291

  100.00%

DNA coding region (bp)

   2,265,747

  92.89%

DNA G+C content (bp)

   1,702,985

  69.81%

Number of replicons

   2

Extrachromosomal elements

   1

Total genes

   2,445

  100.00%

RNA genes

   54

  2.21%

rRNA operons

   2

Protein-coding genes

   2,391

  97.79%

Pseudo genes

   18

  0.74%

Genes with function prediction

   1,709

  69.90%

Genes in paralog clusters

   25

  1.02%

Genes assigned to COGs

   1,772

  72.47%

Genes assigned Pfam domains

   1,842

  75.34%

Genes with signal peptides

   615

  25.15%

Genes with transmembrane helices

   654

  26.75%

CRISPR repeats

   0

Figure 3

Graphical circular map of chromosome (map of plasmid not shown). 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.

Table 4

Number of genes associated with the general COG functional categories

Code

   value

    %age

   Description

J

   150

    7.7

   Translation, ribosomal structure and biogenesis

A

   1

    0.0

   RNA processing and modification

K

   90

    4.6

   Transcription

L

   91

    4.7

   Replication, recombination and repair

B

   1

    0.0

   Chromatin structure and dynamics

D

   27

    1.4

   Cell cycle control, cell division, chromosome partitioning

Y

   0

    0.0

   Nuclear structure

V

   31

    1.6

   Defense mechanisms

T

   80

    4.1

   Signal transduction mechanisms

M

   79

    4.1

   Cell wall/membrane/envelope biogenesis

N

   23

    1.2

   Cell motility

Z

   0

    0.0

   Cytoskeleton

W

   0

    0.0

   Extracellular structures

U

   47

    2.4

   Intracellular trafficking, secretion, and vesicular transport

O

   82

    4.2

   Posttranslational modification, protein turnover, chaperones

C

   154

    7.9

   Energy production and conversion

G

   125

    6.4

   Carbohydrate transport and metabolism

E

   203

    10.4

   Amino acid transport and metabolism

F

   72

    3.7

   Nucleotide transport and metabolism

H

   93

    4.8

   Coenzyme transport and metabolism

I

   66

    3.4

   Lipid transport and metabolism

P

   100

    5.1

   Inorganic ion transport and metabolism

Q

   31

    1.6

   Secondary metabolites biosynthesis, transport and catabolism

R

   244

    12.5

   General function prediction only

S

   155

    8.0

   Function unknown

-

   673

    27.6

   Not in COGs

Declarations

Acknowledgements

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.


This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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