Open Access

Complete genome sequence of Spirochaeta smaragdinae type strain (SEBR 4228T)

  • Konstantinos Mavromatis1,
  • Montri Yasawong2,
  • Olga Chertkov1, 3,
  • Alla Lapidus1,
  • Susan Lucas1,
  • Matt Nolan1,
  • Tijana Glavina Del Rio1,
  • Hope Tice1,
  • Jan-Fang Cheng1,
  • Sam Pitluck1,
  • Konstantinos Liolios1,
  • Natalia Ivanova1,
  • Roxanne Tapia1, 3,
  • Cliff Han1, 3,
  • David Bruce1, 3,
  • Lynne Goodwin1, 3,
  • Amrita Pati1,
  • Ami Chen4,
  • Krishna Palaniappan4,
  • Miriam Land1, 5,
  • Loren Hauser1, 5,
  • Yun-Juan Chang1, 5,
  • Cynthia D. Jeffries1, 5,
  • John C. Detter1, 3,
  • Manfred Rohde2,
  • Evelyne Brambilla6,
  • Stefan Spring6,
  • Markus Göker6,
  • Johannes Sikorski6,
  • Tanja Woyke1,
  • James Bristow1,
  • Jonathan A. Eisen1, 7,
  • Victor Markowitz4,
  • Philip Hugenholtz1,
  • Hans-Peter Klenk6 and
  • Nikos C. Kyrpides1
Standards in Genomic Sciences20103:3020136

https://doi.org/10.4056/sigs.1143106

Published: 31 October 2010

Abstract

Spirochaeta smaragdinae Magot et al. 1998 belongs to the family Spirochaetaceae. The species is Gram-negative, motile, obligately halophilic and strictly anaerobic and is of interest because it is able to ferment numerous polysaccharides. S. smaragdinae is the only species of the family Spirochaetaceae known to reduce thiosulfate or element sulfur to sulfide. This is the first complete genome sequence in the family Spirochaetaceae. The 4,653,970 bp long genome with its 4,363 protein-coding and 57 RNA genes is a part of the Genomic Encyclopedia of Bacteria and Archaea project.

Keywords

spiral shaped corkscrew-like motility chemoorganotroph strictly anaerobe obligately halophile rhodanese-like protein Spirochaetaceae GEBA

Introduction

Strain SEBR 4228T (= DSM 11293 = JCM 15392) is the type strain of the species Spirochaeta smaragdinae. Currently, there are eighteen species [1] and two subspecies in the genus Spirochaeta [1,2]. The generic name derives from the Greek word ‘speira’ meaning ‘a coil’ and the Greek word ‘chaitê’ meaning ‘hair’, referring to the spiral shape of bacterial cell. The species epithet is derived from the Latin word ‘smaragdinae’ meaning ‘from Emerald’, referring to the name Emerald of an oil field in Congo. Strain SEBR 4228T was isolated from an oil-injection production water sample of a Congo offshore oilfield [3] and described in 1997 by Magot et al. as ‘Spirochaeta smaragdinae’ [3]. Here we present a summary classification and a set of features for S. smaragdinae SEBR 4228T, together with the description of the complete genomic sequencing and annotation.

Classification and features

Strain SEBR 4228T shares 82.2–99.0% 16S rRNA gene sequence identity with the type strains from the other members of genus Spirochaeta [4], with the type strain of S. bajacaliforniensis [5], isolated from a mud sample in Laguna Figueroa (Baja California, Mexico) showing the highest degree of sequence similarity (99%). Notwithstanding the high degree of 16S rRNA gene sequence identity, these two strains are characterized by low genomic similarity (38%) in DNA-DNA hybridization studies and differ by numerous differences in carbon source utilization [3]. Several type strains from the genus Treponema show the highest degree of similarity for non-Spirochaeta strains (82.9-83.6%) [4]. A representative genomic 16S rRNA sequence of strain SEBR 4228T was compared using BLAST with the most recent release of the Greengenes database [6] and the relative frequencies of taxa and keywords, weighted by BLAST scores, were determined. The three most frequent genera were Spirochaeta (76.4%), ‘Sphaerochaeta’ (15.8%) and Cytophaga (7.8%). Within the five most frequent keywords in the labels of environmental samples were ‘microbial’ (11.7%), ‘mat’ (10.5%), ‘hypersaline’ (7.7%), and ‘sediment’ (1.7%). The environmental samples database (env_nt) contains the marine metagenome genomic clone 1061006082084 (EK988302) that is 92% identical to the 16S rRNA gene sequence of SEBR 4228T. No phylotypes from genomic surveys could be linked to the species S. smaragdinae or even the genus Spirochaeta, indicating a rather rare occurrence of these in the habitats screened so far (as of August 2010).

Figure 1 shows the phylogenetic neighborhood of S. smaragdinae SEBR 4228T in a 16S rRNA based tree. The sequences of the two 16S rRNA gene copies differ from each other by up to one nucleotide, and differ by up to five nucleotides from the previously published 16S rRNA sequence generated from DSM 11293 (U80597), which contains two ambiguous base calls.
Figure 1.

Phylogenetic tree highlighting the position of S. smaragdinae SEBR 4228T relative to the type strains of the other species within the genus and of the other genera within the genus Spirochaeta. The tree was inferred from 1,385 aligned characters [7,8] of the 16S rRNA gene sequence under the maximum likelihood criterion [9] and rooted in accordance with the current taxonomy [10]. The branches are scaled in terms of the expected number of substitutions per site. Numbers above branches are support values from 500 bootstrap replicates [11] if larger than 60%. Lineages with type strain genome sequencing projects registered in GOLD [12] are shown in blue, published genomes in bold.

Strain SEBR 4228T is a Gram-negative, chemoorganotrophic and strictly anaerobic bacterium with spiral shaped, 0.3–0.5 × 5–30 µm long cells (Figure 2 and Table 1). It possesses a multilayer, crenulating, Gram-negative cell envelope, which consists of an outer membrane and an inner membrane adjoining the cytoplasmic membrane [3]. Sillons, which are the contact point between the protoplasmic cylinder, the inner membrane and the outer membrane, are also observed from the cells of S. smaragdinae SEBR 4228T [3]. Strain SEBR 4228T forms translucent colonies with regular edges (0.5 mm of diameter) after two weeks of incubation on SEM agar plates at 37°C [3]. The strain is motile with a corkscrew-like motion, which is characteristic for the typical 1-2-1 periplasmic flagellar arrangement of the members of the genus Spirochaeta [3]. The periplasmic, non-extracellular location of the flagella make the Spirochaeta a valuable candidate for the study of flagella evolution [26]. The enlarged spherical bodies, which are typical for spirochetes, are also observed in strain SEBR 4228T [3]. The temperature range for growth is from 20°C to 40°C, with an optimum temperature at 37°C [3]. The pH range for growth is between 5.5 and 8.0, with an optimum pH of 7.0 [3]. Strain SEBR 4228T is obligately halophilic [3] and is able to grow on media that contains 1–10% of NaCl, with an optimum salinity at 5% NaCl [3]. Under optimum growth conditions, the doubling time is approximately 25 h in the presence of glucose and thiosulfate [3]. Strain SEBR 4228T is able to utilize biotrypcase, fructose, fumarate, galactose, D-glucose, glycerol, mannitol, mannose, ribose, D-xylose and yeast extract, but not acetate, D-arabinose, butyrate, casamino acids, lactate, maltose, propionate, pyruvate, rhamnose, sorbose, sucrose and L-xylose [3]. Yeast extract is required for growth and cannot be replaced by a vitamin mixture [3]. Strain SEBR 4228T ferments fumarate to acetate and succinate [3]. The major end-product of glucose fermentation of strain SEBR 4228T is lactate with traces of H2 and ethanol [3]. S. smaragdinae is the only species of Spirochaeta known to reduce thiosulfate or elemental sulfur to sulfide [3]. Strain SEBR 4228T produces lactate, acetate, CO2 and H2S as the end-products of glucose oxidation when thiosulfate is present in the growth medium [3]. The strain contains a rhodanese-like protein which expresses rhodanese activity [27]. This enzyme is able to reduce thiosulfate to sulfide [28]. Rhodanese is also widely found in other members of the domain Bacteria [2931].
Figure 2.

Scanning electron micrograph of S. smaragdinae SEBR 4228T

Table 1.

Classification and general features of S. smaragdinae SEBR 4228T according to the MIGS recommendations [13].

MIGS ID

Property

Term

Evidence code

 

Current classification

Domain Bacteria

TAS [14]

 

Phylum Spirochaetae

TAS [15,16]

 

Class Spirochaetes

TAS [16]

 

Order Spirochaetales

TAS [17,18]

 

Family Spirochaetaceae

TAS [18,19]

 

Genus Spirochaeta

TAS [18,2022]

 

Species Spirochaeta smaragdinae

TAS [3,23]

 

Type strain SEBR 4228

TAS [3]

 

Gram stain

negative

TAS [3]

 

Cell shape

spiral

TAS [3]

 

Motility

yes

TAS [3]

 

Sporulation

none

NAS

 

Temperature range

between 20°C and over 40°C

TAS [3]

 

Optimum temperature

37°C

TAS [3]

 

Salinity

1–10% NaCl (optimum 5%)

TAS [3]

MIGS-22

Oxygen requirement

obligately anaerobic

TAS [3]

 

Carbon source

polysaccharides

TAS [3]

 

Energy source

chemoorganotroph

TAS [3]

MIGS-6

Habitat

oil-fields

TAS [3]

MIGS-15

Biotic relationship

free-living

TAS [3]

MIGS-14

Pathogenicity

none

NAS

 

Biosafety level

1

TAS [24]

 

Isolation

oil-injection water sample in the production system of an oil field

TAS [3]

MIGS-4

Geographic location

Emerald oil fields in Congo

TAS [3]

MIGS-5

Sample collection time

1997 or before

TAS [3]

MIGS-4.1

Latitude

not reported

 

MIGS-4.2

Longitude

not reported

 

MIGS-4.3

Depth

not reported

 

MIGS-4.4

Altitude

not reported

 

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.

Chemotaxonomy

No cellular fatty acids profiles are currently available for S. smaragdinae SEBR 4228T. However, C16:0 dimethyl acetate is the major cellular fatty acids of the type strains of the closely related S. dissipatitropha, S. asiatica and S. americana, and C16:0 fatty acid methyl ester is the major cellular fatty acids of S. africana [20,32].

Genome sequencing and annotation

Genome project history

This organism was selected for sequencing on the basis of its phylogenetic position [33], and is part of the Genomic Encyclopedia of Bacteria and Archaea project [34]. The genome project is deposited in the Genome OnLine Database [12] 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: 454 pyrosequence standard and PE (12 kb insert size) libraries and one Illumina standard library

MIGS-29

Sequencing platforms

454 GS FLX Titanium, Illumina GAii

MIGS-31.2

Sequencing coverage

58.8 × pyrosequence, 6.9 × Illumina

MIGS-30

Assemblers

Newbler version 2.0.0-PostRelease-11/04/2008, phrap,

MIGS-32

Gene calling method

Prodigal 1.4, GenePRIMP

 

INSDC ID

CP002116

 

Genbank Date of Release

August 6, 2010

 

GOLD ID

Gc013354

 

NCBI project ID

32637

 

Database: IMG-GEBA

2503128010

MIGS-13

Source material identifier

DSM 11293

 

Project relevance

Tree of Life, GEBA

Growth conditions and DNA isolation

S. smaragdinae SEBR 4228T, DSM 11293, was grown anaerobically in medium 819 (Spirochaeta smaragdinae medium) [35] at 35°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/LALMice for cell lysis as described in Wu et al. [34].

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. Pyrosequencing reads were assembled using the Newbler assembler version 2.0.0-PostRelease-11/04/2008 (Roche). The initial Newbler assembly consisted of 51 contigs in one scaffold 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 was assembled with Velvet [36] and the consensus sequences were shredded into 1.5 kb overlapped fake reads and assembled together with the 454 data. Draft assemblies were based on 273 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 was used for sequence assembly and quality assessment in the following finishing process. After the shotgun stage, reads were assembled with parallel phrap (High Performance Software, LLC). Possible mis-assemblies were corrected with gapResolution, Dupfinisher, or sequencing cloned bridging PCR fragments with subcloning or transposon bombing (Epicentre Biotechnologies, Madison, WI) [37]. Gaps between contigs were closed by editing in Consed, by PCR and by Bubble PCR primer walks (J.-F.Chang, unpublished). A total of 147 additional reactions were necessary to close gaps and to raise the quality of the finished sequence. Illumina reads were also used to improve the final consensus quality using an in-house developed tool - the Polisher [38]. The error rate of the completed genome sequence is 0.2 in 100,000. Together, the combination of the Illumina and 454 sequencing platforms provided 65.7× coverage of the genome.

Genome annotation

Genes were identified using Prodigal [39] as part of the Oak Ridge National Laboratory genome annotation pipeline, followed by a round of manual curation using the JGI GenePRIMP pipeline [40]. 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 [41].

Genome properties

The genome consists of a 4,653,970 bp long chromosome with a 49.0% GC content (Table 3 and Figure 3). Of the 4,363 genes predicted, 4,306 were protein-coding genes, and 57 RNAs; eighty seven pseudogenes were also identified. The majority of the protein-coding genes (74.2%) 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.
Figure 3.

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.

Table 3.

Genome Statistics

Attribute

Value

% of Total

Genome size (bp)

4,653,970

100.00%

DNA coding region (bp)

4,315,215

92.97%

DNA G+C content (bp)

2,278,823

48.97%

Number of replicons

1

 

Extrachromosomal elements

0

 

Total genes

4,363

100.00%

RNA genes

57

1.31%

rRNA operons

2

 

Protein-coding genes

4306

98.69%

Pseudo genes

87

1.99%

Genes with function prediction

3,235

74.15%

Genes in paralog clusters

818

18.75%

Genes assigned to COGs

3,318

76.05%

Genes assigned Pfam domains

3,443

78.91%

Genes with signal peptides

871

26.36%

Genes with transmembrane helices

1,150

22.45%

CRISPR repeats

1

 
Table 4.

Number of genes associated with the general COG functional categories

Code

Value

%age

Description

J

159

4.3

Translation, ribosomal structure and biogenesis

A

0

0.0

RNA processing and modification

K

328

8.8

Transcription

L

129

3.5

Replication, recombination and repair

B

1

0.0

Chromatin structure and dynamics

D

25

0.7

Cell cycle control, cell division, chromosome partitioning

Y

0

0.0

Nuclear structure

V

58

1.6

Defense mechanisms

T

321

8.6

Signal transduction mechanisms

M

183

4.9

Cell wall/membrane/envelope biogenesis

N

94

2.5

Cell motility

Z

0

0.0

Cytoskeleton

W

0

0.0

Extracellular structures

U

58

1.6

Intracellular trafficking and secretion, and vesicular transport

O

114

3.1

Posttranslational modification, protein turnover, chaperones

C

223

6.0

Energy production and conversion

G

553

14.9

Carbohydrate transport and metabolism

E

326

8.8

Amino acid transport and metabolism

F

96

2.6

Nucleotide transport and metabolism

H

130

3.5

Coenzyme transport and metabolism

I

61

1.6

Lipid transport and metabolism

P

165

4.4

Inorganic ion transport and metabolism

Q

30

0.8

Secondary metabolites biosynthesis, transport and catabolism

R

450

12.1

General function prediction only

S

212

5.7

Function unknown

-

1,045

23.9

Not in COGs

Declarations

Acknowledgements

We would like to gratefully acknowledge the help of Maren Schröder (DSMZ) for growing cultures of S. smarasgdinae. 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 and Thailand Research Fund Royal Golden Jubilee Ph.D. Program No. PHD/0019/2548 for MY.

Authors’ Affiliations

(1)
DOE Joint Genome Institute
(2)
HZI - Helmholtz Centre for Infection Research
(3)
Bioscience Division, Los Alamos National Laboratory
(4)
Biological Data Management and Technology Center, Lawrence Berkeley National Laboratory
(5)
Oak Ridge National Laboratory
(6)
DSMZ - German Collection of Microorganisms and Cell Cultures GmbH
(7)
University of California Davis Genome Center

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