Open Access

Complete genome sequence of Corynebacterium pseudotuberculosis biovar ovis strain P54B96 isolated from antelope in South Africa obtained by rapid next generation sequencing technology

  • Syed Shah Hassan1,
  • Luis Carlos Guimarães1,
  • Ulisses de Pádua Pereira5,
  • Arshad Islam6,
  • Amjad Ali1,
  • Syeda Marriam Bakhtiar1,
  • Dayana Ribeiro1,
  • Anderson Rodrigues dos Santos1,
  • Siomar de Castro Soares1,
  • Fernanda Dorella1,
  • Anne Cybelle Pinto1,
  • Maria Paula Cruz Schneider2,
  • Maria Silvanira Barbosa2,
  • Síntia Almeida1,
  • Vinícius Abreu1,
  • Flávia Aburjaile1,
  • Adriana Ribeiro Carneiro2,
  • Louise Teixeira Cerdeira2,
  • Karina Fiaux1,
  • Eudes Barbosa1,
  • Carlos Diniz1,
  • Flavia S. Rocha1,
  • Rommel Thiago Jucá Ramos2,
  • Neha Jain4,
  • Sandeep Tiwari4,
  • Debmalya Barh4,
  • Anderson Miyoshi1,
  • Borna Müller3,
  • Artur Silva2Email author and
  • Vasco Azevedo1
Standards in Genomic Sciences20127:7020189

https://doi.org/10.4056/sigs.3066455

Published: 19 December 2012

Abstract

The Actinobacteria, Corynebacterium pseudotuberculosis strain P54B96, a nonmotile, non-sporulating and a mesophile bacterium, was isolated from liver, lung and mediastinal lymph node lesions in an antelope from South Africa. This strain is interesting in the sense that it has been found together with non-tuberculous mycobacteria (NTMs) which could nevertheless play a role in the lesion formation. In this work, we describe a set of features of C. pseudotuberculosis P54B96, together with the details of the complete genome sequence and annotation. The genome comprises of 2.34 Mbp long, single circular genome with 2,084 protein-coding genes, 12 rRNA, 49 tRNA and 62 pseudogenes and a G+C content of 52.19%. The analysis of the genome sequence provides means to better understanding the molecular and genetic basis of virulence of this bacterium, enabling a detailed investigation of its pathogenesis.

Keywords

biovar ovis Gram-positive pathogen caseous lymphadenitis/cheesy gland disease liver lesion Antelope genome sequencing Ion Torrent

Introduction

Caseous lymphadenitis (CLA) or cheesy gland [1] is highly prevalent in many regions of the world, resulting in huge and significant economic losses in agribusiness since it is responsible for a decrease in wool production and carcass quality [2]. Mainly small ruminant populations like sheep and goats, and other mammals, such as bovines, pigs, deer, ovines, equines, and even, though rarely, in camels and humans, are the victims of Corynebacterium pseudotuberculosis [36]. The disease is characterized by the presence of caseous necrosis in external and/or internal lymph nodes [1,7]. Ulcerative lymphangitis, which is confined to the lymph vessels of extremities particularly the hind legs, is a disease caused by this bacterium in the horse [8,9]. The bacterium in some cases of human lymphadenitis, clinical strains are occasionally recovered [10]. The prevalence of CLA in the animals scattered throughout the globe needs effective measures to control the onset of the disease in herds along with the treatment of infected animals. Numerous reports have been published worldwide where mainly small ruminants are the carriers of the C. pseudotuberculosis. They include South Africa, Brazil, United States of America, Canada, Australia, New Zealand, United Kingdom and Egypt [1118]. Histopathological examination of antelope carcasses from a South African game reserve, a part of their routine meat inspection, showed tuberculosis-like lesions. These lesions were characterized by the presence of encapsulated necrogranulomatous inflammation similar to CLA within the pulmonary tissues, in bronchial lymph nodes, liver, kidney and some other organs of the antelopes [11]. Diseases caused by the bacterium C. pseudotuberculosis are presented in various clinical forms as sheep and goats, affected with CLA [19]. Among the affected animal population, the increased prevalence and rapid transmission of the disease necessitates certain measures to control disease dissemination and prevent the nearby wildlife. The analysis of the genome sequence will help us better understand the molecular and genetic basis of virulence of this bacterium.

Classification and Features

C. pseudotuberculosis is a facultative intracellular pathogen showing pleomorphic forms like coccoids and filamentous rods, with sizes ranging between 0.5–0.6 µm and 1.0–3.0 µm [2]. Cells are described as Gram-positive, non-encapsulated, non-motile, non-sporulating and possessing fimbriae [12,20]. The bacterium was first isolated in 1888 from bovine farcy by Nocard and was first completely described by Preisz, showing its resemblance to diphtheria bacillus. The organism has been previously named Bacillus pseudotuberculosis ovis; Bacillus pseudotuberculosi and, Corynebacterium ovis [8,21]. It is a facultative anaerobe. The best growth temperature and pH are 37° C and 7.0–7.2, respectively [17,22]. After initially growing sparsely, strain P54B96 forms organized clumps on the agar surface, demonstrating dry opaque and concentrically ringed colonies. In liquid media it develops a granular deposit with a surface pellicle [8,22,23].

There exist two biotypes of C. pseudotuberculosis according to their capability of nitrate reduction. Bacteria capable of performing the reduction of nitrate are classified into biovar equi (nitrate reduction positive; mainly isolated from horses and cattle) while the bacteria which can not perform the reduction of nitrate, pertain to biovar ovis (nitrate reduction negative; frequently isolated from sheep and goats) [2,24]. Corynebacteria possess an unusual structural organization in their cell envelope, similar to the Gram-negative bacteria [25] and belong to a very heterogeneous CMNR (Corynebacterium, Mycobacterium, Nocardia and Rhodococcus) group that shares characteristics including an outer lipid layer, mycolic acids in the cell wall along with with its derivatives including phospholipids and lipomannans [4]. Marchand et al. (2012) and others reported the presumed mycomembrane, an atypical outer membrane, pore-forming proteins like PorA and PorB, mycoloyltransferases, the so-called fibronectin-binding proteins like cMytA-D and cMytF, several lipoproteins and some unknown putative C-terminal hydrophobic anchored proteins [26]. Analysis of amino acids and amino sugars of cell wall peptidoglycan reveals the presence of meso-diaminopimelic acid (meso-DAP). Major cell wall sugars are arabinose and galactose [17,27]. In addition, high and low molecular mass glucan, arabinomannan and lipoglycan also make part of the cell wall. Trehalose dimycolate (TDM) and trehalose monomycolate (TMM) are soluble cell envelope lipids [28]. Biochemically, all strains produce acid from glucose, maltose, fructose, sucrose and mannose [21,22]. This bacterium is catalase positive and phospholipase D, beta-hemolysis and oxidase negative [23,29].

Figure 1 shows the phylogenetic neighborhood of C. pseudotuberculosis strain P54B96 in an rpoB gene (β subunit of RNA polymerase) based tree. It has recently been shown that phylogenetic analysis for the identification of Corynebacterium as well as other CMNR species based on rpoB gene sequences are more accurate than analyses based on 16S rRNA [42,43]. The rpoB gene sequences of reference strains from the CMNR group were used to construct the phylogenetic tree.
Figure 1.

Phylogenetic tree of C. pseudotuberculosis strain P54B96 representing its position relative to type strains in Corynebacteriaceae along with some other type strains of CMNR group. The tree was inferred from 3,537 aligned characters of the rpoB gene sequence using maximum likelihood method and then checked for its agreement with the current classification Table 1. The branch lengths represent the expected number of substitutions per site. Numbers adjacent to the branches are support values from 1,000 bootstrap replicates, indicated when Larger than 60%. Calculations to determine the phylogenetic distances were done by the software MEGA v5 [30].

Genome sequencing and annotation

Genome project history

This organism was selected for sequencing on the basis of its phylogenetic position. The genome project is deposited in the Genomes OnLine Database [44] and the complete genome sequence is available in GenBank (CP003385.1). Sequencing, finishing and annotation were performed by the Rede Paraense de Genômica e Proteômica (RPGP), Pará, Brazil. A summary of the project information is shown in Table 2.

Growth conditions and DNA isolation

C. pseudotuberculosis P54B96 was grown in brain-heart-infusion broth (BHI-HiMedia Laboratories Pvt. Ltda, India) in shake culture at140 rpm and at 37°C. Extraction of chromosomal DNA was performed by using 50 mL of 48–72 h culture of C. pseudotuberculosis, centrifuged at 4°C and 2000× g for 20 min. Re-suspension of cell pellets was done in 1 mL Tris/EDTA/NaCl [10 mM Tris/HCl (pH7.0), 10 mM EDTA (pH8.0), and 300 mM NaCl] for re-centrifugation under the same conditions. The pellets were re-suspended in 1 mL TE/lysozyme [25 mM Tris/HCl (pH8.0), 10 mM EDTA (pH8.0), 10 mM NaCl, and 10 mg lysozyme/mL]. The sample was then incubated at 37°C for 30 min and then 30 µL of 30% (w/v) sodium N-lauroyl-sarcosine (Sarcosyl) was added to it, incubated for 20 min at 65°C, followed by incubation for 5 min at 4°C. Purification of DNA with phenol/chloroform/isoamylalcohol (25:24:1) was followed by precipitation with ethanol. DNA concentration was determined by spectrophotometer, and the DNA was visualized in ethidium bromide-stained 0.7% agarose gel.

Genome sequencing and assembly

The complete genome sequence of C. pseudotuberculosis P54B96 was obtained using the Ion Torrent PGM (Life Technologies) Sequencing Platform. A total, of 562,812 reads were generated, each with a mean size of 112 nts usable sequence (35-fold coverage). Furthermore, a hybrid de novo assembly approach was applied using 376,642 Ion filtered reads (19-fold coverage). This was carried out after quality filtering process during which reads representing an average Phred quality of less than 20, were removed. This strategy allowed closing gaps without bench work time cost [45].
Table 1.

Classification and general features of C. pseudotuberculosis strain P54B96 according to the MIGS recommendations [31].

MIGS ID

Property

Term

Evidence code

 

Classification

Domain Bacteria

TAS [32]

  

Phylum Actinobacteria

TAS [33]

  

Class Actinobacteria

TAS [34]

  

Order Actinomycetales

TAS [3437]

  

Suborder Corynebacterineae

 
  

Family Corynebacteriaceae

TAS [34,35,37,38]

  

Genus Corynebacterium

TAS [35,38,39]

  

Species Corynebacterium pseudotuberculosis

TAS [35,40]

  

Strain P54B96

TAS [11]

 

Gram stain

Positive

TAS [21]

 

Cell shape

pleomorphic forms

TAS [21]

 

Motility

non-motile

TAS [8]

 

Sporulation

non-sporulating

TAS [22]

 

Temperature range

mesophilic

TAS [8,22]

 

Optimum temperature

37°C

TAS [8,22]

 

Salinity

not reported

NAS

MIGS-22

Oxygen requirement

aerobic and facultatively anaerobic

TAS [8,22]

 

Carbon source

glucose, fructose, maltose, mannose, and sucrose

TAS [8]

 

Energy source

Chemoorganotroph

TAS [8]

MIGS-6

Habitat

Host

TAS [22]

MIGS-15

Biotic relationship

intracellular facultative pathogen

TAS [22]

MIGS-14

Pathogenicity

sheep, goats, horses and cattle, rarely humans

TAS [5,6]

 

Biosafety level

2

TAS [22]

 

Isolation

liver, lung, mediastinal lymph node lesions of antelope

TAS [11]

MIGS-4

Geographic location

Mpumalanga province, South Africa

TAS [11]

MIGS-5

Sample collection time

2009

TAS [11]

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 the Gene Ontology project [41]. 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.

Table 2.

Genome sequencing project information

MIGS ID

Property

Term

MIGS-31

Finishing quality

Finished

MIGS-28

Libraries used

Fragments (mean size 112 bp)

MIGS-29

Sequencing platforms

Semiconductor Ion Torrent PGM

MIGS-31.2

Sequencing coverage

35-fold

MIGS-30

Assemblers

CLC Genome Workbench 4.7.2, Velvet

MIGS-32

Gene calling method

Glimmer v3.02

 

INSDC ID

CP003385 (chromosome)

 

GenBank Date of Release

April 05, 2012

 

GOLD ID

Gc02176

 

NCBI project ID

77871

 

Database: IMG-GEBA

2512564058

MIGS-13

Source material identifier

BHI broth, P54B96

 

Project relevance

Animal Pathogen, Medical

For homopolymer correction, an inherent problem of the Ion Torrent [46], CLCBio Genome Workbench 4.7.2 was used. Having detected a high number of frameshifts, manual curation was required prior to analysis to prevent false-positive identification of pseudogenes. The genome of P54B96 strain consists of 2,337,657 bp circular chromosome and the average G+C content of the chromosome is 52.2%. The genome was predicted to contain 2,084 coding sequences (CDS), four rRNA operons, 49 tRNA and 62 pseudogenes.

Genome annotation

For automatic annotation, different programs were used. These include; Glimmer: gene predictor [47], RNAmmer: rRNA predictor [48]; tRNA-scan-SE: tRNA predictor [49]; and Tandem Repeat Finder: repetitive DNA predictor [50]. Functional annotation was performed by similarity analyses, using public databases of National Center for Biotechnology Information (NCBI) non-redundant database, Pfam and InterProScan software [51], which integrates multiple domain and protein family databases. Manual annotation was performed using Artemis [52].

Metabolic network analysis

The metabolic Pathway/Genome Database (PGDB) was computationally generated using Pathway Tools software version 15.0 [53] and MetaCyc version 15.0 [54], based on annotated EC numbers and a customized enzyme name mapping file. There has been no manual curation in the database and it may contain errors, similar to a Tier 3 BioCyc PGDB [55].

Genome properties

The genome is 2,337,657 bp long and comprises one main circular chromosome with a 52.19% GC content. A total of 2,207 genes were predicted, among which 2,146 were protein coding genes, and 61 RNAs; 62 pseudogenes were also identified. Of the whole genome, 69.01% comprise genes that were assigned with putative functions, while the remaining genes were annotated as hypothetical proteins. The properties and statistics of the C. pseudotuberculosis genome are listed in Table 3. The distributions of genes into COGs functional categories is presented in Figure 2 and Table 4, followed by a cellular overview diagram in Figure 3 and a summary of metabolic network statistics shown in Table 5.
Figure 2.

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.

Figure 3.

Schematic cellular overview of all pathways of the C. pseudotuberculosis P54B96 metabolism. Nodes represent metabolites, with shape indicating class of metabolite. Lines represent reactions.

Table 3.

Genome Statistics

Attribute

Value

% of Total

Genome size (bp)

2,337,657

100.00%

DNA coding region (bp)

2,005,391

85.79%

DNA G+C content (bp)

1,219,912

52.19%

Number of replicons

1

 

Extrachromosomal elements

0

 

Total genes

2,145

100.00%

RNA genes

61

2.76%

rRNA operons

4

 

Protein-coding genes

2,084

97.16%

Pseudo genes

62

2.81%

Genes with function prediction

1,511

68.46%

Genes in paralog clusters

425

19.26%

Genes assigned to COGs

1,552

70.32%

Genes assigned Pfam domains

1,596

72.32%

Genes with signal peptides

651

29.50%

Genes with transmembrane helices

584

26.46%

CRISPR repeats

0

 
Table 4.

Number of genes associated with the general COG functional categories

Code

Value

%age

Description

J

140

6.72

Translation, ribosomal structure and biogenesis

A

1

0.1

RNA processing and modification

K

121

5.8

Transcription

L

88

4.2

Replication, recombination and repair

B

0

0.0

Chromatin structure and dynamics

D

21

1.0

Cell cycle control, cell division, chromosome partitioning

Y

0

0.0

Nuclear structure

V

25

1.2

Defense mechanisms

T

54

2.6

Signal transduction mechanisms

M

87

4.2

Cell wall/membrane biogenesis

N

1

0.1

Cell motility

Z

0

0.0

Cytoskeleton

W

0

0.0

Extracellular structures

U

27

1.3

Intracellular trafficking and secretion

O

77

3.7

Posttranslational modification, protein turnover, chaperones

C

90

4.3

Energy production and conversion

G

113

5.4

Carbohydrate transport and metabolism

E

177

8.5

Amino acid transport and metabolism

F

73

3.5

Nucleotide transport and metabolism

H

102

4.9

Coenzyme transport and metabolism

I

57

2.7

Lipid transport and metabolism

P

122

5.9

Inorganic ion transport and metabolism

Q

26

1.3

Secondary metabolites biosynthesis, transport and catabolism

R

169

8.1

General function prediction only

S

136

6.5

Function unknown

-

655

31.4

Not in COGs

Table 5.

Metabolic Network Statistics

Attribute

Value

Total genes

2,145

Enzymes

500

Enzymatic reactions

764

Metabolic pathways

152

Metabolites

622

Declarations

Acknowledgements

We would like to gratefully acknowledge the help of all the team members & the financing agencies. Hassan S.S acknowledges the receipt of a Scholarship from the CNPq under the “TWAS-CNPq Postgraduate Fellowship Programme” for doctoral studies. This work was partially executed by Rede Paraense de Genômica e Proteômica supported by FAPESPA (Fundação de Amparo à Pesquisa do Estado do Pará), CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brasil), CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasil) and FAPEMIG (Fundação de Amparo à Pesquisa do Estado de Minas Gerais, Brasil).

Authors’ Affiliations

(1)
Laboratório de Genética Celular e Molecular, Departamento de Biologia Geral, Instituto de Ciências Biológicas (ICB), Universidade Federal de Minas Gerais
(2)
Instituto de Ciências Biológicas, Universidade Federal do Pará
(3)
DST/NRF Centre of Excellence for Biomedical Tuberculosis Research/MRC Centre for Molecular and Cellular Biology, Division of Molecular Biology and Human Genetics, Faculty of Health Sciences, Stellenbosch University
(4)
Centre for Genomics and Applied Gene Technology, Institute of Integrative Omics and Applied Biotechnology (IIOAB)
(5)
Departamento de Medicina Veterinária, Universidade Federal de Lavras
(6)
Instituto de Ciências Exatas (ICEX), Universidade Federal de Minas Gerais

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