Abstract
The systematic application of next-generation DNA sequencing technologies has provided detailed insights into the genomics of corynebacteria. The genomes of 13 Corynebacterium diphtheriae strains isolated from cases of classical diphtheria, endocarditis and pneumonia were completely sequenced and annotated, providing first insights into the pan-genome of this species. Comparative gene content analyses revealed an enormous collection of variable pilus gene clusters relevant for adhesion properties of C. diphtheriae. Variation in the distributed genome is apparently a common strategy of C. diphtheriae to establish differences in host-pathogen interactions. Molecular data deduced from the complete genome sequences of two Corynebacterium ulcerans strains provided considerable knowledge of candidate virulence factors, including a novel type of ribosome-binding protein with striking structural similarity to Shiga-like toxins. Likewise, functional data deduced from the complete genome sequences of six Corynebacterium pseudotuberculosis isolates from various sources greatly extended the knowledge of virulence factors and indicated that this species is equipped with a distinct gene set promoting its survival under unfavorable environmental conditions encountered in the mammalian host.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA (2011) BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 12:402
Barksdale WL, Pappenheimer AM Jr (1954) Phage-host relationships in nontoxigenic and toxigenic diphtheria bacilli. J Bacteriol 67:220–232
Blom J, Albaum SP, Doppmeier D, Pühler A, Vorhölter FJ, Zakrzewski M, Goesmann A (2009) EDGAR: a software framework for the comparative analysis of prokaryotic genomes. BMC Bioinformatics 10:154
Brüssow H, Canchaya C, Hardt WD (2004) Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68:560–602
Bukovska G, Klucar L, Vlcek C, Adamovic J, Turna J, Timko J (2006) Complete nucleotide sequence and genome analysis of bacteriophage BFK20—a lytic phage of the industrial producer Brevibacterium flavum. Virology 348:57–71
Cerdeira LT, Carneiro AR, Ramos RT, Almeida SS de, D’Afonseca V, Schneider MP, Baumbach J, Tauch A, McCulloch JA, Azevedo VA, Silva A (2011a) Rapid hybrid de novo assembly of a microbial genome using only short reads: Corynebacterium pseudotuberculosis I19 as a case study. J Microbiol Methods 86:218–223
Cerdeira LT, Pinto AC, Schneider MP, Almeida SS de, Santos AR dos, Barbosa EG, Ali A, Barbosa MS, Carneiro AR, Ramos RT, Oliveira RS de, Barh D, Barve N, Zambare V, Belchior SE, Guimarães LC, Castro SS de, Dorella FA, Rocha FS, Abreu VA de, Tauch A, Trost E, Miyoshi A, Azevedo V, Silva A (2011b) Whole-genome sequence of Corynebacterium pseudotuberculosis PAT10 strain isolated from sheep in Patagonia, Argentina. J Bacteriol 193:6420–6421
Cerdeira LT, Schneider MP, Pinto AC, Almeida SS de, Santos AR dos, Barbosa EG, Ali A, Aburjaile FF, Abreu VA de, Guimarães LC, Castro SS de, Dorella FA, Rocha FS, Bol E, Gomes deSPH, Lopes TS, Barbosa MS, Carneiro AR, Jucá Ramos RT, Coimbra NA, Lima AR, Barh D, Jain N, Tiwari S, Raja R, Zambare V, Ghosh P, Trost E, Tauch A, Miyoshi A, Azevedo V, Silva A (2011c) Complete genome sequence of Corynebacterium pseudotuberculosis strain CIP 52.97, isolated from a horse in Kenya. J Bacteriol 193:7025–7026
Cerdeño-Tarrága AM, Efstratiou A, Dover LG, Holden MT, Pallen M, Bentley SD, Besra GS, Churcher C, James KD, De Zoysa A, Chillingworth T, Cronin A, Dowd L, Feltwell T, Hamlin N, Holroyd S, Jagels K, Moule S, Quail MA, Rabbinowitsch E, Rutherford KM, Thomson NR, Unwin L, Whitehead S, Barrell BG, Parkhill J (2003) The complete genome sequence and analysis of Corynebacterium diphtheriae NCTC13129. Nucleic Acids Res 31:6516–6523
Collin M, Fischetti VA (2004) A novel secreted endoglycosidase from Enterococcus faecalis with activity on human immunoglobulin G and ribonuclease B. J Biol Chem 279:22558–22570
D’Afonseca V, Soares SC, Ali A, Santos AR, Pinto AC, Magalhães AA, Faria CJ, Barbosa E, Guimarães LC, Eslabão M, Almeida SS, Abreu VA, Zerlotini A, Carneiro AR, Cerdeira LT, Ramos RT, Hirata R Jr, Mattos-Guaraldi AL, Trost E, Tauch A, Silva A, Schneider MP, Miyoshi A, Azevedo V (2012) Reannotation of the Corynebacterium diphtheriae NCTC13129 genome as a new approach to studying gene targets connected to virulence and pathogenicity in diphtheria. Open Access Bioinformatics 4:1–13
Deveau H, Garneau JE, Moineau S (2010) CRISPR/Cas system and its role in phage-bacteria interactions. Annu Rev Microbiol 64:475–93
Dias AA, Silva FC Jr, Pereira GA, Souza MC, Camello TC, Damasceno JA, Pacheco LG, Miyoshi A, Azevedo VA, Hirata R Jr, Bôas MH, Mattos-Guaraldi AL (2010) Corynebacterium ulcerans isolated from an asymptomatic dog kept in an animal shelter in the metropolitan area of Rio de Janeiro, Brazil. Vector Borne Zoonotic Dis 10:743–748
Dittmann S, Wharton M, Vitek C, Ciotti M, Galazka A, Guichard S, Hardy I, Kartoglu U, Koyama S, Kreysler J, Martin B, Mercer D, Ronne T, Roure C, Steinglass R, Strebel P, Sutter R, Trostle M. 2000. Successful control of epidemic diphtheria in the states of the Former Union of Soviet Socialist Republics: lessons learned. J Infect Dis. 181:10–22
Dorella FA, Pacheco LG, Oliveira SC, Miyoshi A, Azevedo V (2006a) Corynebacterium pseudotuberculosis: microbiology, biochemical properties, pathogenesis and molecular studies of virulence. Vet. Res 37:201–218
Dorella FA, Fachin MS, Billault A, Dias Neto E, Soravito C, Oliveira SC, Meyer R, Miyoshi A, Azevedo V (2006b) Construction and partial characterization of a Corynebacterium pseudotuberculosis bacterial artificial chromosome library through genomic survey sequencing. Genet Mol Res 5:653–663
Droege M, Hill B (2008) The Genome Sequencer FLX System—longer reads, more applications, straight forward bioinformatics and more complete datasets. J. Biotechnol 136:3–10
Freeman VJ (1951) Studies on the virulence of bacteriophage-infected strains of Corynebacterium diphtheriae. J Bacteriol 61:675–688
Halachev MR, Loman NJ, Pallen MJ (2011) Calculating orthologs in bacteria and archaea: a divide and conquer approach. PLoS One 6:e28388
Hirata R Jr, Souza SM, Rocha-de-Souza CM, Andrade AF, Monteiro-Leal LH, Formiga LC, Mattos-Guaraldi AL (2004) Patterns of adherence to HEp-2 cells and actin polymerisation by toxigenic Corynebacterium diphtheriae strains. Microb Pathog 36:125–130
Hogg RA, Wessels J, Hart J, Efstratiou A, De Zoysa A, Mann G, Allen T, Pritchard GC (2009) Possible zoonotic transmission of toxigenic Corynebacterium ulcerans from companion animals in a human case of fatal diphtheria. Vet Rec 165:691–692
Iwaki M, Komiya T, Yamamoto A, Ishiwa A, Nagata N, Arakawa Y, Takahashi M (2010) Genome organization and pathogenicity of Corynebacterium diphtheriae C7(–) and PW8 strains. Infect Immun 78:3791–3800
Jolley KA, Chan MS, Maiden MC (2004) mlstdbNet – distributed multi-locus sequence typing (MLST) databases. BMC Bioinformatics 5:86
Kunkle CA, Schmitt MP (2005) Analysis of a DtxR-regulated iron transport and siderophore biosynthesis gene cluster in Corynebacterium diphtheriae. J Bacteriol 187:422–433
LaPointe P, Wei X, Gariepy J (2005) A role for the protease-sensitive loop region of Shiga-like toxin 1 in the retrotranslocation of its A1 domain from the endoplasmic reticulum lumen. J Biol Chem 280:23310–23318
Lewis CM Jr, Obregón-Tito A, Tito RY, Foster MW, Spicer PG (2012) The Human Microbiome Project: lessons from human genomics. Trends Microbiol 20:1–4
Mandlik A, Swierczynski A, Das A, Ton-That H (2007) Corynebacterium diphtheriae employs specific minor pilins to target human pharyngeal epithelial cells. Mol Microbiol 64:111–124
Mardis ER (2008) Next-generation DNA sequencing methods. Annu Rev Genom Hum Genet 9:387–402
Marraffini LA, Sontheimer EJ (2010) CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat Rev Genet 11:181–190
Mattos-Guaraldi AL, Sampaio JL, Santos CS, Pimenta FP, Pereira GA, Pacheco LG, Miyoshi A, Azevedo V, Moreira LO, Gutierrez FL, Costa JL, Costa-Filho R, Damasco PV, Camello TC, Hirata R Jr (2008) First detection of Corynebacterium ulcerans producing a diphtheria-like toxin in a case of human with pulmonary infection in the Rio de Janeiro metropolitan area, Brazil. Mem Inst Oswaldo Cruz 103:396–400
McKean SC, Davies JK, Moore RJ (2007) Expression of phospholipase D, the major virulence factor of Corynebacterium pseudotuberculosis, is regulated by multiple environmental factors and plays a role in macrophage death. Microbiology 153:2203–2211
Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R (2005) The microbial pan-genome. Curr Opin Genet Dev 15:589–594
Mokrousov I (2009) Corynebacterium diphtheriae: genome diversity, population structure and genotyping perspectives. Infect Genet Evol 9:1–15
Mokrousov I, Narvskaya O, Limeschenko E, Vyazovaya A (2005) Efficient discrimination within a Corynebacterium diphtheriae epidemic clonal group by a novel macroarray-based method. J Clin Microbiol 43:1662–1668
Morozova O, Marra MA (2008) Applications of next-generation sequencing technologies in functional genomics. Genomics 92:255–264
O’Loughlin EV, Robins-Browne RM (2001) Effect of Shiga toxin and Shiga-like toxins on eukaryotic cells. Microbes Infect 3:493–507
Ott L, Höller M, Rheinlaender J, Schäffer TE, Hensel M, Burkovski A (2010) Strain-specific differences in pili formation and the interaction of Corynebacterium diphtheriae with host cells. BMC Microbiol 10:257
Pagani I, Liolios K, Jansson J, Chen IM, Smirnova T, Nosrat B, Markowitz VM, Kyrpides NC. 2012. The Genomes OnLine Database (GOLD) v.4: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res. 40:D571–579.
Park WH, Williams AW (1896) The production of diphtheria toxin. J Exp Med 1:164–185
Qian Y, Lee JH, Holmes RK (2002) Identification of a DtxR-regulated operon that is essential for siderophore-dependent iron uptake in Corynebacterium diphtheriae. J Bacteriol 184:4846–4856
Rappuoli R, Michel JL, Murphy JR (1983) Restriction endonuclease map of corynebacteriophage γc tox + isolated from the Park-Williams no. 8 strain of Corynebacterium diphtheriae. J Virol 45:524–530
Ratti G, Covacci A, Rappuoli R (1997) A tRNA2 Arg gene of Corynebacterium diphtheriae is the chromosomal integration site for toxinogenic bacteriophages. Mol Microbiol 25:1179–1181
Rogers EA, Das A, Ton-That H (2011) Adhesion by pathogenic corynebacteria. Adv Exp Med Biol 715:91–103
Rothberg JM, Leamon JH (2008) The development and impact of 454 sequencing. Nat Biotechnol 26:1117–1124
Ruiz JC, D’Afonseca V, Silva A, Ali A, Pinto AC, Santos AR, Rocha AA, Lopes DO, Dorella FA, Pacheco LG, Costa MP, Turk MZ, Seyffert N, Moraes PM, Soares SC, Almeida SS, Castro TL, Abreu VA, Trost E, Baumbach J, Tauch A, Schneider MP, McCulloch J, Cerdeira LT, Ramos RT, Zerlotini A, Dominitini A, Resende DM, Coser EM, Oliveira LM, Pedrosa AL, Vieira CU, Guimarães CT, Bartholomeu DC, Oliveira DM, Santos FR, Rabelo ÉM, Lobo FP, Franco GR, Costa AF, Castro IM, Dias SR, Ferro JA, Ortega JM, Paiva LV, Goulart LR, Almeida JF, Ferro MI, Carneiro NP, Falcão PR, Grynberg P, Teixeira SM, Brommonschenkel S, Oliveira SC, Meyer R, Moore RJ, Miyoshi A, Oliveira GC, Azevedo V (2011) Evidence for reductive genome evolution and lateral acquisition of virulence functions in two Corynebacterium pseudotuberculosis strains. PLoS One 6:e18551
Salzberg SL (2007) Genome re-annotation: a wiki solution? Genome Biol 8:102
Schröder J, Maus I, Meyer K, Wördemann S, Blom J, Jaenicke S, Schneider J, Trost E, Tauch A (2012) Complete genome sequence, lifestyle, and multi-drug resistance of the human pathogen Corynebacterium resistens DSM 45100 isolated from blood samples of a leukemia patient. BMC Genomics 13:141
Shendure J, Ji H (2008) Next-generation DNA sequencing. Nat Biotechnol 26:1135–1145
Silva A, Schneider MP, Cerdeira L, Barbosa MS, Ramos RT, Carneiro AR, Santos R, Lima M, D’Afonseca V, Almeida SS, Santos AR, Soares SC, Pinto AC, Ali A, Dorella FA, Rocha F, Abreu VA de, Trost E, Tauch A, Shpigel N, Miyoshi A, Azevedo V (2011) Complete genome sequence of Corynebacterium pseudotuberculosis I19, a strain isolated from a cow in Israel with bovine mastitis. J Bacteriol 193:323–324
Soares SC, Dorella FA, Pacheco LG, R. Hirata R Jr, Mattos-Guaraldi AL, Azevedo V, Miyoshi A (2011) Plasticity of Corynebacterium diphtheriae pathogenicity islands revealed by PCR. Genet Mol Res 10:1290–1294
Soares SC, Abreu VA, Ramos RT, Cerdeira L, Silva A, Baumbach J, Trost E, Tauch A, Hirata R Jr, Mattos-Guaraldi AL, Miyoshi A, Azevedo V (2012) PIPS: Pathogenicity Island Prediction Software. PLoS One 7:e30848
Soriano F, Tauch A (2008) Microbiological and clinical features of Corynebacterium urealyticum: urinary tract stones and genomics as the Rosetta Stone. Clin Microbiol Infect 14:632–643
Tauch A, Trost E, Tilker A, Ludewig U, Schneiker S, Goesmann A, Arnold W, Bekel T, Brinkrolf K, Brune I, Götker S, Kalinowski J, Kamp PB, Lobo FP, Viehoever P, Weisshaar B, Soriano F, Dröge M, Pühler A (2008a) The lifestyle of Corynebacterium urealyticum derived from its complete genome sequence established by pyrosequencing. J Biotechnol 136:11–21
Tauch A, Schneider J, Szczepanowski R, Tilker A, Viehoever P, Gartemann KH, Arnold W, Blom J, Brinkrolf K, Brune I, Götker S, Weisshaar B, Goesmann A, Dröge M, Pühler A (2008b) Ultrafast pyrosequencing of Corynebacterium kroppenstedtii DSM44385 revealed insights into the physiology of a lipophilic corynebacterium that lacks mycolic acids. J Biotechnol 136:22–30
Tettelin H, Riley D, Cattuto C, Medini D (2008) Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 11:472–477
Ton-That H, Schneewind O (2003) Assembly of pili on the surface of Corynebacterium diphtheriae. Mol Microbiol 50:1429–1438
Trost E, Götker S, Schneider J, Schneiker-Bekel S, Szczepanowski R, Tilker A, Viehoever P, Arnold W, Bekel T, Blom J, Gartemann KH, Linke B, Goesmann A, Pühler A, Shukla SK, Tauch A (2010a) Complete genome sequence and lifestyle of black-pigmented Corynebacterium aurimucosum ATCC 700975 (formerly C. nigricans CN-1) isolated from a vaginal swab of a women with spontaneous abortion. BMC Genomics 11:91
Trost E, L O, Schneider J, Schröder J, Jaenicke S, Goesmann A, Husemann P, Stoye J, Dorella FA, Rocha FS, Castro SS de, D’Afonseca V, Miyoshi A, Ruiz J, Silva A, Azevedo V, Burkovski A, Guiso N, Join-Lambert OF, Kayal S, Tauch A (2010b) The complete genome sequence of Corynebacterium pseudotuberculosis FRC41 isolated from a 12-year-old girl with necrotizing lymphadenitis reveals insights into gene-regulatory networks contributing to virulence. BMC Genomics 11:728
Trost E, Al-Dilaimi A, Papavasiliou P, Schneider J, Viehoever P, Burkovski A, Soares SC, Almeida SS, Dorella FA, Miyoshi A, Azevedo V, Schneider MP, Silva A, Santos CS, Santos LS, Sabbadini P, Dias AA, Hirata R Jr, Mattos-Guaraldi AL, Tauch A (2011) Comparative analysis of two complete Corynebacterium ulcerans genomes and detection of candidate virulence factors. BMC Genomics 12:383
Trost E, Blom J, Castro SS de, Huang IH, Al-Dilaimi A, Schröder J, Jaenicke S, Dorella FA, Rocha FS, Miyoshi A, Azevedo V, Schneider MP, Silva A, Camello TC, Sabbadini PS, Santos CS, Santos LS, Hirata R Jr, Mattos-Guaraldi AL, Efstratiou A, Schmitt MP, Ton-That H, Tauch A (2012) Pangenomic study of Corynebacterium diphtheriae that provides insights into the genomic diversity of pathogenic isolates from cases of classical diphtheria, endocarditis, and pneumonia. J Bacteriol 194:3199–3215
Acknowledgement
The authors thank Siomar de Castro Soares for bioinformatic support, running the PIPS pipeline, and visualizing comparative genomic data with the BRIG software.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer Science+Business Media Dordrecht (outside the USA)
About this chapter
Cite this chapter
Trost, E., Tauch, A. (2014). Comparative Genomics and Pathogenicity Islands of Corynebacterium diphtheriae, Corynebacterium ulcerans, and Corynebacterium pseudotuberculosis . In: Burkovski, A. (eds) Corynebacterium diphtheriae and Related Toxigenic Species. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7624-1_3
Download citation
DOI: https://doi.org/10.1007/978-94-007-7624-1_3
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-7623-4
Online ISBN: 978-94-007-7624-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)