Skip to main content
Top
Published in: Gut Pathogens 1/2016

Open Access 01-12-2016 | Genome report

Complete genome sequence of Peptoclostridium difficile strain Z31

Authors: Felipe L. Pereira, Carlos A. Oliveira Júnior, Rodrigo O. S. Silva, Fernanda A. Dorella, Alex F. Carvalho, Gabriel M. F. Almeida, Carlos A. G. Leal, Francisco C. F. Lobato, Henrique C. P. Figueiredo

Published in: Gut Pathogens | Issue 1/2016

Login to get access

Abstract

Background

Peptoclostridium (Clostridium) difficile is a spore-forming bacterium responsible for nosocomial infections in humans. It is recognized as an important agent of diarrhea and colitis in several animal species and a possible zoonotic agent. Despite the known importance of P. difficile infection in humans and animals, no vaccine or other effective measure to control the disease is commercially available. A possible alternative treatment for P. difficile infection is the use of a nontoxigenic strain of P. difficile as a competitive exclusion agent. However, a thorough knowledge of this strain is necessary for this purpose. We selected P. difficile Z31, a nontoxigenic strain (PCR ribotype 009), for investigation because it prevents P. difficile infection in a hamster model.

Results

The genome sequence of P. difficile Z31 is a circular chromosome of 4298,263 bp, with a 29.21 % GC content, encoding 4128 proteins, and containing 78 pseudogenes. This strain belongs to ST 3, clade 1, and has five phage regions in its genome. Genes responsible for resistance to tetracycline and erythromycin were detected and more importantly, Z31 also contains genes that promote spore production and stability, cell attachment, intestinal adherence, and biofilm formation.

Conclusion

In this study, we present the first complete genome sequence of nontoxigenic P. difficile strain Z31. When the Z31 genome was compared with those of other isolates available in GenBank, including a draft genome of a nontoxigenic strain, several unique regions were evident. Z31 contains no toxin genes, but encodes several non-toxin virulence factors, which may favor host colonization.
Appendix
Available only for authorised users
Literature
2.
go back to reference Skerman VBD, Mcgowan V, Sneath PHA. Approved Lists of Bacterial Names. Int J Syst Bacteriol. 1980;30:225–420.CrossRef Skerman VBD, Mcgowan V, Sneath PHA. Approved Lists of Bacterial Names. Int J Syst Bacteriol. 1980;30:225–420.CrossRef
3.
go back to reference Prévot AR. Études de systématique bactérienne IV. Critique de la conception actuelle du genre Clostridium. In: Cato EP, Hash DE, Holdeman LV et al, editors. Electrophoretic study of Clostridium species. J Clin Microbiol. 1982;15:668–702. Prévot AR. Études de systématique bactérienne IV. Critique de la conception actuelle du genre Clostridium. In: Cato EP, Hash DE, Holdeman LV et al, editors. Electrophoretic study of Clostridium species. J Clin Microbiol. 1982;15:668–702.
6.
go back to reference George RH, Symonds JM, Dimock F, Brown JD, Arabi Y, Shinagawa N, Keighley MR, Alexander-Williams J, Burdon DW. Identification of Clostridium difficile as a cause of pseudomembranous colitis. Br Med J. 1978;1:695.CrossRefPubMedPubMedCentral George RH, Symonds JM, Dimock F, Brown JD, Arabi Y, Shinagawa N, Keighley MR, Alexander-Williams J, Burdon DW. Identification of Clostridium difficile as a cause of pseudomembranous colitis. Br Med J. 1978;1:695.CrossRefPubMedPubMedCentral
7.
go back to reference Larson HE, Price AB, Honour P, Borrielo SP. Clostridium difficile and the aetiology of pseudomembranous colitis. Lancet. 1978;1:1063–6.CrossRefPubMed Larson HE, Price AB, Honour P, Borrielo SP. Clostridium difficile and the aetiology of pseudomembranous colitis. Lancet. 1978;1:1063–6.CrossRefPubMed
9.
go back to reference Ogielska M, Lanotte P, Le Brun C, Valentin AS, Garot D, Tellier AC, Halimi JM, Colombat P, Guilleminault L, Lioger B, Vegas H, De Toffol B, Constans T, Bernard L. Emergence of community-acquired Clostridium difficile infection: the experience of a French hospital and review of the literature. Int J Infect Dis. 2015. doi:10.1016/j.ijid.2015.06.007.PubMed Ogielska M, Lanotte P, Le Brun C, Valentin AS, Garot D, Tellier AC, Halimi JM, Colombat P, Guilleminault L, Lioger B, Vegas H, De Toffol B, Constans T, Bernard L. Emergence of community-acquired Clostridium difficile infection: the experience of a French hospital and review of the literature. Int J Infect Dis. 2015. doi:10.​1016/​j.​ijid.​2015.​06.​007.PubMed
11.
go back to reference Silva RO, D’Elia ML, Teixeira ÉP, Pereira PL, de Magalhaes Soares DF, Cavalcanti ÁR, Kocuvan A, Rupnik M, Santos AL, Junior CA, Lobato FC. Clostridium difficile and Clostridium perfringens from wild carnivore species in Brazil. Anaerobe. 2014;31(28):207–11.CrossRef Silva RO, D’Elia ML, Teixeira ÉP, Pereira PL, de Magalhaes Soares DF, Cavalcanti ÁR, Kocuvan A, Rupnik M, Santos AL, Junior CA, Lobato FC. Clostridium difficile and Clostridium perfringens from wild carnivore species in Brazil. Anaerobe. 2014;31(28):207–11.CrossRef
14.
go back to reference Songer JG, Anderson MA. Clostridium difficile: an important pathogen of food animals. Anaerobe. 2006;12(1):1–4.CrossRefPubMed Songer JG, Anderson MA. Clostridium difficile: an important pathogen of food animals. Anaerobe. 2006;12(1):1–4.CrossRefPubMed
18.
go back to reference Songer JG, Jones R, Anderson MA, Barbara AJ, Post KW, Trinha HT. Prevention of porcine Clostridium difficile-associated disease by competitive exclusion with nontoxigenic organisms. Vet Microbiol. 2007. doi:10.1016/j.vetmic.2007.04.019. Songer JG, Jones R, Anderson MA, Barbara AJ, Post KW, Trinha HT. Prevention of porcine Clostridium difficile-associated disease by competitive exclusion with nontoxigenic organisms. Vet Microbiol. 2007. doi:10.​1016/​j.​vetmic.​2007.​04.​019.
19.
go back to reference Merrigan MM, Sambol SP, Johnson S, Gerding DN. New approach to the management of Clostridium difficile infection: colonisation with non-toxigenic C. difficile during daily ampicillin or ceftriaxone administration. Int J Antimicrob Agents. 2009. doi:10.1016/S0924-8579(09)70017-2.PubMed Merrigan MM, Sambol SP, Johnson S, Gerding DN. New approach to the management of Clostridium difficile infection: colonisation with non-toxigenic C. difficile during daily ampicillin or ceftriaxone administration. Int J Antimicrob Agents. 2009. doi:10.​1016/​S0924-8579(09)70017-2.PubMed
20.
go back to reference Villano SA, Seiberling M, Tatarowicz W, Monnot-Chase E, Gerding DN. Evaluation of an oral suspension of VP20621, spores of nontoxigenic Clostridium difficile strain M3, in healthy subjects. Antimicrob Agents Chemother. 2012. doi:10.1128/AAC.00913-12.PubMedPubMedCentral Villano SA, Seiberling M, Tatarowicz W, Monnot-Chase E, Gerding DN. Evaluation of an oral suspension of VP20621, spores of nontoxigenic Clostridium difficile strain M3, in healthy subjects. Antimicrob Agents Chemother. 2012. doi:10.​1128/​AAC.​00913-12.PubMedPubMedCentral
21.
go back to reference Nagaro KJ, Phillips ST, Cheknis AK, Sambol SP, Zukowski WE, Johnson S, Gerdinga DN. Nontoxigenic Clostridium difficile protects hamsters against challenge with historic and epidemic strains of toxigenic BI/NAP1/027 C. difficile. Antimicrob Agents Chemother. 2013. doi:10.1128/AAC.00580-13.PubMedPubMedCentral Nagaro KJ, Phillips ST, Cheknis AK, Sambol SP, Zukowski WE, Johnson S, Gerdinga DN. Nontoxigenic Clostridium difficile protects hamsters against challenge with historic and epidemic strains of toxigenic BI/NAP1/027 C. difficile. Antimicrob Agents Chemother. 2013. doi:10.​1128/​AAC.​00580-13.PubMedPubMedCentral
22.
go back to reference Oliveira CA, Silva ROS, Diniz NA, Pires PS, Lobato FCF, Assis RA. Prevention of Clostridium difficile infection in hamsters using a non-toxigenic strain. Cienc Rural. 2016. doi:10.1590/0103-8478cr20150454. Oliveira CA, Silva ROS, Diniz NA, Pires PS, Lobato FCF, Assis RA. Prevention of Clostridium difficile infection in hamsters using a non-toxigenic strain. Cienc Rural. 2016. doi:10.​1590/​0103-8478cr20150454.
23.
go back to reference Sambol SP, Merrigan MM, Tang JK, Johnson S, Gerding DN. Colonization for the prevention of Clostridium difficile disease in Hamsters. J Infect Dis. 2002. doi:10.1086/345676.PubMed Sambol SP, Merrigan MM, Tang JK, Johnson S, Gerding DN. Colonization for the prevention of Clostridium difficile disease in Hamsters. J Infect Dis. 2002. doi:10.​1086/​345676.PubMed
25.
go back to reference Chevreux B, Wetter T, Suhai S. Genome sequence assembly using trace signals and additional sequence information. Comput Sci Biol Proc Ger Conf Bioinform. 1999;99:45–56. Chevreux B, Wetter T, Suhai S. Genome sequence assembly using trace signals and additional sequence information. Comput Sci Biol Proc Ger Conf Bioinform. 1999;99:45–56.
26.
go back to reference Nurk S, Bankevich A, Antipov D, et al. Assembling genomes and mini-metagenomes from highly chimeric reads. Res Comput Mol Biol. 2013;7821:158–70.CrossRef Nurk S, Bankevich A, Antipov D, et al. Assembling genomes and mini-metagenomes from highly chimeric reads. Res Comput Mol Biol. 2013;7821:158–70.CrossRef
29.
go back to reference Rutherford K, Parkhill J, Crook J, et al. Artemis: sequence visualization and annotation. Bioinformatics. 2000;16:944–5.CrossRefPubMed Rutherford K, Parkhill J, Crook J, et al. Artemis: sequence visualization and annotation. Bioinformatics. 2000;16:944–5.CrossRefPubMed
31.
go back to reference Sonnhammer EL, von Heijne G, Krogh A. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol. 1998;6:175–82.PubMed Sonnhammer EL, von Heijne G, Krogh A. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol. 1998;6:175–82.PubMed
36.
go back to reference Hennequin C, Porcheray F, Waligora-Dupriet A, Collignon A, Barc M, Bourlioux P, Karjalainen T. GroEL (Hsp60) of Clostridium difficile is involved in cell adherence. Microbiology. 2001;147(Pt 1):87–96.CrossRefPubMed Hennequin C, Porcheray F, Waligora-Dupriet A, Collignon A, Barc M, Bourlioux P, Karjalainen T. GroEL (Hsp60) of Clostridium difficile is involved in cell adherence. Microbiology. 2001;147(Pt 1):87–96.CrossRefPubMed
38.
go back to reference Lin Y, Kuo C, Koleci X, McDonough SP, Chang Y. Manganese binds to Clostridium difficile Fbp68 and is essential for fibronectin binding. J Biol Chem. 2011. doi:10.1074/jbc.M110.184523. Lin Y, Kuo C, Koleci X, McDonough SP, Chang Y. Manganese binds to Clostridium difficile Fbp68 and is essential for fibronectin binding. J Biol Chem. 2011. doi:10.​1074/​jbc.​M110.​184523.
39.
40.
go back to reference Ðapa T, Leuzzi R, Ng YK, Baban ST, Adamo R, Kuehna SA, Scarselli M, Minton NP, Serruto D, Unnikrishnan M. Multiple factors modulate biofilm formation by the anaerobic pathogen Clostridium difficile. J Bacteriol. 2013. doi:10.1128/JB.01980-12.PubMedPubMedCentral Ðapa T, Leuzzi R, Ng YK, Baban ST, Adamo R, Kuehna SA, Scarselli M, Minton NP, Serruto D, Unnikrishnan M. Multiple factors modulate biofilm formation by the anaerobic pathogen Clostridium difficile. J Bacteriol. 2013. doi:10.​1128/​JB.​01980-12.PubMedPubMedCentral
43.
go back to reference Permpoonpattana P, Phetcharaburanin J, Mikelsone A, Dembek M, Tan S, Brisson MC, Ragione R, Brisson AR, Fairweather N, Hong HA, Cutting SM. Functional characterization of Clostridium difficile spore coat proteins. J Bacteriol. 2013. doi:10.1128/JB.02104-12.PubMedPubMedCentral Permpoonpattana P, Phetcharaburanin J, Mikelsone A, Dembek M, Tan S, Brisson MC, Ragione R, Brisson AR, Fairweather N, Hong HA, Cutting SM. Functional characterization of Clostridium difficile spore coat proteins. J Bacteriol. 2013. doi:10.​1128/​JB.​02104-12.PubMedPubMedCentral
44.
go back to reference Jump RLP, Pultz MJ, Donskey CJ. Vegetative Clostridium difficile survives in room air on moist surfaces and in gastric contents with reduced acidity: a potential mechanism to explain the association between proton pump inhibitors ans C. difficile-associated diarrhea? Antimicrob Agents Chemother. 2007. doi:10.1128/AAC.01443-06.PubMedPubMedCentral Jump RLP, Pultz MJ, Donskey CJ. Vegetative Clostridium difficile survives in room air on moist surfaces and in gastric contents with reduced acidity: a potential mechanism to explain the association between proton pump inhibitors ans C. difficile-associated diarrhea? Antimicrob Agents Chemother. 2007. doi:10.​1128/​AAC.​01443-06.PubMedPubMedCentral
46.
go back to reference Spigaglia P, Barbanti F, Mastrantonio P. Detection of a genetic linkage between genes coding for resistance to tetracycline and erythromycin in Clostridium difficile. Microb Drug Resist. 2007. doi:10.1089/mdr.2007.723.PubMed Spigaglia P, Barbanti F, Mastrantonio P. Detection of a genetic linkage between genes coding for resistance to tetracycline and erythromycin in Clostridium difficile. Microb Drug Resist. 2007. doi:10.​1089/​mdr.​2007.​723.PubMed
47.
go back to reference Persson S, Torpdahl M, Olsen KEP. New multiplex PCR method for the detection of Clostridium difficile toxin A (tcdA) and toxin B (tcdB) and the binary toxin (cdtA/cdtB) genes applied to a Danish strain collection. Clin Microbiol Infect. 2008. doi:10.1111/j.1469-0691.2008.02092.x. Persson S, Torpdahl M, Olsen KEP. New multiplex PCR method for the detection of Clostridium difficile toxin A (tcdA) and toxin B (tcdB) and the binary toxin (cdtA/cdtB) genes applied to a Danish strain collection. Clin Microbiol Infect. 2008. doi:10.​1111/​j.​1469-0691.​2008.​02092.​x.
48.
go back to reference Dingle KE, Elliot B, Robinson E, Griffiths D, Eyre DW, Stoesser N, Vaughan A, Golubchik T, Fawley WN, Wilcox MH, Peto TE, Walker AS, Riley TV, Crook DW, Didelot X. Evolutionary history of the Clostridium difficile pathogenicity locus. Genome Biol Evol. 2014. doi:10.1093/gbe/evt204.PubMedCentral Dingle KE, Elliot B, Robinson E, Griffiths D, Eyre DW, Stoesser N, Vaughan A, Golubchik T, Fawley WN, Wilcox MH, Peto TE, Walker AS, Riley TV, Crook DW, Didelot X. Evolutionary history of the Clostridium difficile pathogenicity locus. Genome Biol Evol. 2014. doi:10.​1093/​gbe/​evt204.PubMedCentral
49.
go back to reference Agren J, Sundström A, Håfström T, Segerman B. Gegenees: fragmented alignment of multiple genomes for determining phylogenomic distances and genetic signatures unique for specified target groups. PLoS One. 2012;7:e39107.CrossRefPubMedPubMedCentral Agren J, Sundström A, Håfström T, Segerman B. Gegenees: fragmented alignment of multiple genomes for determining phylogenomic distances and genetic signatures unique for specified target groups. PLoS One. 2012;7:e39107.CrossRefPubMedPubMedCentral
53.
go back to reference Kurka H, Ehrenreich A, Ludwig W, Monot M, Rupnik M, Barbut F, Indra A, Dupuy B, Liebl W. Sequence similarity of Clostridium difficile strains by analysis of conserved genes and genome content is reflected by their ribotype affiliation. PLoS One. 2014. doi:10.1371/journal.pone.0086535.PubMedPubMedCentral Kurka H, Ehrenreich A, Ludwig W, Monot M, Rupnik M, Barbut F, Indra A, Dupuy B, Liebl W. Sequence similarity of Clostridium difficile strains by analysis of conserved genes and genome content is reflected by their ribotype affiliation. PLoS One. 2014. doi:10.​1371/​journal.​pone.​0086535.PubMedPubMedCentral
54.
go back to reference Darling AE, Worden P, Chapman TA, Chowdhury PR, Charles IG, Djordjevic SP. The genome of Clostridium difficile 5.3. Gut Pathogens. 2014. doi:10.1186/1757-4749-6-4. Darling AE, Worden P, Chapman TA, Chowdhury PR, Charles IG, Djordjevic SP. The genome of Clostridium difficile 5.3. Gut Pathogens. 2014. doi:10.​1186/​1757-4749-6-4.
55.
go back to reference Galperin MY, Makarova KS, Wolf YI, Koonin EVA. Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucl Acids Res. 2015. doi:10.1093/nar/gku1223. Galperin MY, Makarova KS, Wolf YI, Koonin EVA. Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucl Acids Res. 2015. doi:10.​1093/​nar/​gku1223.
Metadata
Title
Complete genome sequence of Peptoclostridium difficile strain Z31
Authors
Felipe L. Pereira
Carlos A. Oliveira Júnior
Rodrigo O. S. Silva
Fernanda A. Dorella
Alex F. Carvalho
Gabriel M. F. Almeida
Carlos A. G. Leal
Francisco C. F. Lobato
Henrique C. P. Figueiredo
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2016
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-016-0095-3

Other articles of this Issue 1/2016

Gut Pathogens 1/2016 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.