Open Access

Complete genome sequence of Capnocytophaga ochracea type strain (VPI 2845T)

  • Konstantinos Mavrommatis1,
  • Sabine Gronow2,
  • Elizabeth Saunders1, 3,
  • Miriam Land1, 4,
  • Alla Lapidus1,
  • Alex Copeland1,
  • Tijana Glavina Del Rio1,
  • Matt Nolan1,
  • Susan Lucas1,
  • Feng Chen1,
  • Hope Tice1,
  • Jan-Fang Cheng1,
  • David Bruce1, 3,
  • Lynne Goodwin1, 3,
  • Sam Pitluck1,
  • Amrita Pati1,
  • Natalia Ivanova1,
  • Amy Chen5,
  • Krishna Palaniappan5,
  • Patrick Chain1, 6,
  • Loren Hauser1, 4,
  • Yun-Juan Chang1, 4,
  • Cynthia D. Jeffries1, 4,
  • Thomas Brettin1, 3,
  • John C. Detter1, 3,
  • Cliff Han1, 3,
  • James Bristow1,
  • Markus Göker2,
  • Manfred Rohde7,
  • Jonathan A. Eisen1, 8,
  • Victor Markowitz5,
  • Nikos C. Kyrpides1,
  • Hans-Peter Klenk2 and
  • Philip Hugenholtz1
Standards in Genomic Sciences20091:1020101

https://doi.org/10.4056/sigs.15195

Published: 29 September 2009

Abstract

Capnocytophaga ochracea (Prévot et al. 1956) Leadbetter et al. 1982 is the type species of the genus Capnocytophaga. It is of interest because of its location in the Flavobacteriaceae, a genomically not yet charted family within the order Flavobacteriales. The species grows as fusiform to rod shaped cells which tend to form clumps and are able to move by gliding. C. ochracea is known as a capnophilic (CO2-requiring) organism with the ability to grow under anaerobic as well as aerobic conditions (oxygen concentration larger than 15%), here only in the presence of 5% CO2. Strain VPI 2845T, the type strain of the species, is portrayed in this report as a gliding, Gram-negative bacterium, originally isolated from a human oral cavity. Here we describe the features of this organism, together with the complete genome sequence, and annotation. This is the first completed genome sequence from the flavobacterial genus Capnocytophaga, and the 2,612,925 bp long single replicon genome with its 2193 protein-coding and 59 RNA genes is a part of the Genomic Encyclopedia of Bacteria and Archaea project.

Keywords

glidingcapnophilicperiodontitisgingivitis Flavobacteriaceae

Introduction

Strain VPI 2845T (= DSM 7271 = ATCC 27872 = JCM 1296) is the type strain of Capnocytophaga ochracea, and the type species of the genus Capnocytophaga. C. ochracea was first described by Prévot et al. [1] as ‘Fusiformis nucleatus var. ochraceus’ and later renamed by Leadbetter et al [2]. Other synonyms for C. ochracea are ‘Bacteroides oralis var. elongatus’ [3], ‘Bacteroides ochraceus’ (basonym) [4] and “Ristella ochraceus” (sic) [5]. The organism is of significant interest for its position in the tree of life where the genus Capnocytophaga (8 species) is located within the large family of the Flavobacteriaceae. First, Leadbetter et al. placed the genus Capnocytophaga in the family of the Cytophagaceae within the order Cytophagales [6] which was emended in 2002 by the Subcommittee on the Taxonomy of Flavobacterium and Cytophaga-like bacteria of the International Committee on Systematics of Prokaryotes [7]. C. ochracea is most often found in association with animal and human hosts. In general, it is a normal inhabitant of the human mouth and other non-oral sites. C. ochracea is associated with juvenile and adult periodontitis [8,9] and may cause severe infections in immunocompromised as well as in immunocompetent patients [1012]. Among these are endocarditis, endometritis, osteomyelitis, abscesses, peritonitis, and keratitis. Here we present a summary classification and a set of features for C. ochracea VPI 2845T together with the description of the complete genomic sequence and annotation.

Classification and features

Genbank lists 16S rRNA sequences for only a few small number of cultivated strains belonging to C. ochraceae, all of them isolated from human oral cavity (e.g. U41351, U41353, DQ012332). Phylotypes (sequences from uncultivated bacteria) closely linked to C. ochracea also originate in almost exclusively from human oral samples collected from European, American, Asian and African samples (AF543292, AF543298, AY278613, AM420149, AY429469, FJ470418). Only two bacterial clones are reported from non-human sources. One was isolated from Strongylocentrotus intermedius (sea urchin) in the Sea of Japan (EU432412, EU432438), and the second from Oncorhynchus mykiss (rainbow trout) caught in Scotland (AM179907). Screening of environmental genomic samples and surveys reported at the NCBI BLAST server indicated no closely related phylotypes (>91% sequence identity) that can be linked to the species or genus.

Figure 1 shows the phylogenetic neighborhood of C. ocharcea VPI 2845T in a 16S rRNA based tree. All four 16S rRNA gene copies in the genome of strain VPI 2845T are identical, but differ by two nucleotides from the previously published 16S rRNA sequence (U41350) generated from ATCC 27872.
Figure 1.

Phylogenetic tree highlighting the position of C. ochracea VP 2845T relative to the other type strains of species within the genus Capnocytophaga and to selected type strains of species belonging to other genera within the Flavobacteriaceae. The tree was inferred from 1,405 aligned characters [13,14] of the 16S rRNA gene sequence under the maximum likelihood criterion [15] and rooted with Joostella and Galbibacter. 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 if larger than 60%. Lineages with type strain genome sequencing projects registered in GOLD [16] are shown in blue, published genomes in bold.

C. ochracea is Gram-negative, has no flagellae and is motile by gliding (Table 1, Figure 2). Cells are pigmented and the name ‘ochracea’ is derived from the yellow color exhibited by harvested cell mass [6]. It is a catalase- and oxidase-negative species. C. ochracea is usually susceptible to a number of antibiotics, however, resistance is increasing in this species [23,24]. Furthermore, C. ochracea is known to possess an immunosuppressive factor [25]. All strains of C. ochracea are capable of fermenting glucose, sucrose, maltose and mannose, whereas most strains ferment amygdalin, fructose, galactose, lactose and raffinose [20]. The optimal growth temperature is 37°C. Nitrate is reduced to nitrite, and dextran, glycogen, starch and aesculin are hydrolysed by most strains. Indole is not produced. Acetic and succinic acid are the main metabolic end products of fermentation [6].
Figure 2.

Scanning electron micrograph of C. ochracea VPI 2845T

Table 1.

Classification and general features of C. ochracea VPI 2845T in accordance to the MIGS recommendations [17]

MIGS ID

Property

Term

Evidence code

 

Current classification

Domain Bacteria

TAS [18]

 

Phylum ‘Bacteroidetes

TAS [19]

 

Class Flavobacteria

TAS [19]

 

Order Flavobacteriales

TAS [7]

 

Family Flavobacteriaceae

TAS [7]

 

Genus Capnocytophaga

TAS [6]

 

Species Capnocytophaga ochracea

TAS [6]

 

Type strain VPI 2845

TAS [6]

 

Gram stain

negative

TAS [6]

 

Cell shape

fusiform rods

TAS [6]

 

Motility

gliding

TAS [6]

 

Sporulation

non-sporulating

TAS [6]

 

Temperature range

mesophile

NAS

 

Optimum temperature

30–37°C

NAS

 

Salinity

nonhalophile capnophilic; aerobic or anaerobic with at least

NAS

MIGS-22

Oxygen requirement

5% CO2

TAS [6]

 

Carbon source

glucose, maltose, lactose, sucrose

TAS [20]

 

Energy source

chemoorganotroph, carbohydrates

NAS

MIGS-6

Habitat

human oral cavity

TAS [3]

MIGS-15

Biotic relationship

unknown

NAS

MIGS-14

Pathogenicity

opportunistic pathogen

TAS [12]

 

Biosafety level

2

TAS [21]

 

Isolation

human oral cavity

TAS [2]

MIGS-4

Geographic location

not reported

 

MIGS-5

Sample collection time

not reported

 

MIGS-4.1

   

MIGS-4.2

Latitude - 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 the Gene Ontology project [22]. If the evidence code is IDA, then the property was directly observed for a living isolate by one of the authors or an expert mentioned in the acknowledgements.

Chemotaxonomy

Analysis of amino acids and amino sugars of the peptidoglycan revealed that glucosamine, muramic acid, D-glutamic acid, alanine, and diaminopimelic acid were the principal components and the peptidoglycan belongs to the Alγ-type. Serine and glycine were not found [26]. As in other Capnocytophaga strains, the fatty acid pattern of strain C. ochracea VPI 2845T is dominated by iso-branched chain saturated fatty acids i-C15:0 (63.5%), C18:2 (8.1%) and i-3OH C17:0 (13.8%) [23,27,28]. Phosphatidylethanolamine and an ornithine-amino lipid were identified as dominating polar lipids, as well as lesser amounts of lysophosphatidyl-ethanolamine [29]. In addition, the unusual sulfonolipid capnine (2-amino-3-hydroxy-15-methylhexadecane-1-sulfonic acid) was identified as major cell wall component [30].

Genome sequencing and annotation

Genome project history

This organism was selected for sequencing on the basis of its phylogenetic position, and is part of the Genomic Encyclopedia of Bacteria and Archaea project. The genome project is deposited in the Genomes OnLine Database [10] and the complete genome sequence in GenBank (CP001632). 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

Two Sanger libraries: 6.5kb pMCL200 and fosmid pcc1Foslibraries and one 454 pyrosequence standard library

MIGS-29

Sequencing platforms

ABI3730, 454GS FLX

MIGS-31.2

Sequencing coverage

9.9× Sanger; 25.2× pyrosequence

MIGS-20

Assemblers

Newbler, phrap

MIGS-32

Gene calling method

Prodigal, GenePrimp

 

INSDC / Genbank ID

CP001632

 

Genbank Date of Release

August 26, 2009

 

GOLD ID

Gc01027

 

NCBI project ID

29403

 

Database: IMG-GEBA

2501416900

MIGS-13

Source material identifier

DSM 7271

 

Project relevance

Tree of Life, GEBA, Medical

Growth conditions and DNA isolation

C. ochracea VPI 2845T, DSM 7271, was grown under anaerobic conditions in DSMZ medium 340 (Capnocytophaga Medium, [31]) plus 0.1% NaHCO3 at 37°C. DNA was isolated from 1–1.5 g of cell paste using Qiagen Genomic 500 DNA Kit (Qiagen, Hilden, Germany) with a modified protocol, L, for cell lysis, as described in Wu et al. [32].

Genome sequencing and assembly

The genome was sequenced using a combination of Sanger and 454 sequencing platforms. All general aspects of library construction and sequencing performed at the JGI can be found at the JGI website. 454 Pyrosequencing reads were assembled using the Newbler assembler version 1.1.02.15 (Roche). Large Newbler contigs were broken into 2,919 overlapping fragments of 1,000 bp and entered into assembly as pseudo-reads. The sequences were assigned quality scores based on Newbler consensus q-scores with modifications to account for overlap redundancy and to adjust inflated q-scores. A hybrid 454/Sanger assembly was made using the parallel phrap assembler (High Performance Software, LLC). Possible mis-assemblies were corrected with Dupfinisher or transposon bombing of bridging clones [33]. Gaps between contigs were closed by editing in Consed, custom primer walk or PCR amplification. A total of 226 Sanger finishing reads were produced to close gaps, to resolve repetitive regions, and to raise the quality of the finished sequence. The error rate of the completed genome sequence is less than 1 in 100,000. Together all sequence types provided 35.1× coverage of the genome.

Genome annotation

Genes were identified using Prodigal [34] as part of the Oak Ridge National Laboratory genome annotation pipeline, followed by a round of manual curation using the JGI GenePRIMP pipeline [35]. 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 were performed within the Integrated Microbial Genomes Expert Review (IMG-ER) platform [36].

Genome properties

The genome is 2,612,925 bp long and comprises one circular chromosome with a 39.6% GC content (Table 3). Of the 2,252 genes predicted, 2,193 were protein coding genes, and 59 RNAs; 22 pseudogenes were also identified. Genes assigned with putative functions comprised 61.7% of the genome, while the remaining genes were annotated as hypothetical proteins. The properties and the statistics of the genome are summarized in Table 3. The distribution of genes into COG functional categories is presented in Figure 3 and 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)

2,612,925

100.00%

DNA Coding region (bp)

2,293,132

87.76%

DNA G+C content (bp)

1,034,404

39.59%

Number of replicons

1

 

Extrachromosomal elements

0

 

Total genes

2,252

100.00%

RNA genes

59

2.62%

rRNA operons

4

 

Protein-coding genes

2,193

97.38%

Pseudo genes

22

0.98%

Genes with function prediction

1,403

62.3%

Genes in paralog clusters

207

9.19%

Genes assigned to COGs

1,330

59.06%

Genes assigned Pfam domains

1,379

61.23%

Genes with signal peptides

602

26.73%

Genes with transmembrane helices

471

20.91%

CRISPR repeats

1

 
Table 4.

Number of genes associated with the general COG functional categories

Code

value

%age

Description

J

134

6.1

Translation

A

0

0.0

RNA processing and modification

K

55

2.5

Transcription

L

83

3.8

Replication, recombination and repair

B

0

0.0

Chromatin structure and dynamics

D

19

0.9

Cell cycle control, mitosis and meiosis

Y

0

0.0

Nuclear structure

V

34

1.6

Defense mechanisms

T

35

1.6

Signal transduction mechanisms

M

158

7.2

Cell wall/membrane biogenesis

N

7

0.3

Cell motility

Z

0

0.0

Cytoskeleton

W

0

0.0

Extracellular structures

U

35

1.6

Intracellular trafficking and secretion

O

61

2.8

Posttranslational modification, protein turnover, chaperones

C

69

3.1

Energy production and conversion

G

97

4.4

Carbohydrate transport and metabolism

E

90

4.1

Amino acid transport and metabolism

F

56

2.6

Nucleotide transport and metabolism

H

84

3.8

Coenzyme transport and metabolism

I

53

2.4

Lipid transport and metabolism

P

80

3.6

Inorganic ion transport and metabolism

Q

25

1.1

Secondary metabolites biosynthesis, transport and catabolism

R

145

6.6

General function prediction only

S

100

4.6

Function unknown

-

863

39.4

Not in COGs

Declarations

Acknowledgements

We would like to gratefully acknowledge the help of Sabine Welnitz for growing C. ochracea cultures and Susanne Schneider for DNA extraction and quality analysis (both at DSMZ). 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, well as German Research Foundation (DFG) INST 599/1-1.

Authors’ Affiliations

(1)
DOE Joint Genome Institute
(2)
DSMZ - German Collection of Microorganisms and Cell Cultures GmbH
(3)
Bioscience Division, Los Alamos National Laboratory
(4)
Oak Ridge National Laboratory
(5)
Biological Data Management and Technology Center, Lawrence Berkeley National Laboratory
(6)
Lawrence Livermore National Laboratory
(7)
HZI - Helmholtz Centre for Infection Research
(8)
University of California Davis Genome Center

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Copyright

© The Author(s) 2009