Cookies Notification

We use cookies to improve your website experience. To learn about our use of cookies and how you can manage your cookie settings, please see our Cookie Policy.
×

Abstract

Pasteurella multocida causes acute/chronic pasteurellosis in porcine, resulting in considerable economic losses globally. The draft genomes of two Indian strains NIVEDIPm17 (serogroup D) and NIVEDIPm36 (serogroup A) were sequenced. A total of 2182–2284 coding sequences (CDSs) were predicted along with 5–6 rRNA and 45–46 tRNA genes in the genomes. Multilocus sequence analysis and LPS genotyping showed the presence of ST50: genotype 07 and ST74: genotype 06 in NIVEDIPm17 and NIVEDIPm36, respectively. Pangenome analysis of 61 strains showed the presence of 1653 core genes, 167 soft core genes, 750 shell genes, and 1820 cloud genes. Analysis of virulence-associated genes in 61 genomes indicated the presence of nanB, exbB, exbD, ptfA, ompA, ompH, fur, plpB, fimA, sodA, sodC, tonB, and omp87 in all strains. The 61 genomes contained genes encoding tetracycline (54%), streptomycin (48%), sulphonamide (28%), tigecycline (25%), chloramphenicol (21%), amikacin (7%), cephalosporin (5%), and trimethoprim (5%) resistance. Multilocus sequence type revealed that ST50 was the most common (34%), followed by ST74 (26%), ST13 (24%), ST287 (5%), ST09 (5%), ST122 (3%), and ST07 (2%). Single-nucleotide polymorphism and core genome-based phylogenetic analysis clustered the strains into three major clusters. In conclusion, we described the various virulence factors, mobile genetic elements, and antimicrobial resistance genes in the pangenome of P. multocida of porcine origin, besides the rare presence of LPS genotype 7 in serogroup D.

Get full access to this article

View all available purchase options and get full access to this article.

References

Ahrenfeldt J., Skaarup C., Hasman H., Pedersen A.G., Aarestrup F.M., Lund O. 2017. Bacterial whole genome-based phylogeny: construction of a new benchmarking dataset and assessment of some existing methods. BMC Genom. 18: 19.
Alikhan N.F., Petty N.K., Zakour N.L.B., Beatson S.A. 2011. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genom. 12: 1–10.
Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., et al. 2000. Gene ontology: tool for the unification of biology. Nat Gen. 25: 25–29.
Avram O., Rapoport D., Portugez S., Pupko T. 2019. M1CR0B1AL1Z3R—a user-friendly web server for the analysis of large-scale microbial genomics data. Nucleic Acids Res. 47: 88–92.
Aziz R.K., Bartels D., Best A.A., DeJongh M., Disz T., Edwards R.A., et al. 2008. The RAST Server: rapid annotations using subsystems technology. BMC Genom. 9(1): 1–15.
Bisgaard M., Petersen A., Christensen H. 2013. Multilocus sequence analysis of Pasteurella multocida demonstrates a type species under development. Microbiology, 159: 580–590.
Bolger A.M., Lohse M., Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30: 2114–2120.
Cao P., Guo D., Liu J., Jiang Q., Xu Z., Qu L. 2017. Genome-wide analyses reveal genes subject to positive selection in Pasteurella multocida. Front. Microbiol. 8: 961.
Carter G.R. 1955. Studies on Pasteurella multocida. I. A hemagglutination test for the identification of serological types. Am. J. Vet. Res. 16: 481–484.
Casjens S. 2003. Prophages and bacterial genomics: what have we learned so far? Mol. Microbiol. 49: 277–300.
Christensen H., Sajid S.M., Bisgaard M., Magistrali C.F., Massacci F.R., Liman M., et al. 2022. Prediction of Pasteurella multocida serotypes based on whole genomic sequences. Vet. Microbiol. 271: 109492.
Davis J.J., Wattam A.R., Aziz R.K., Brettin T., Butler R., Butler R.M., Stevens R. 2020. The PATRIC Bioinformatics resource center: expanding data and analysis capabilities. Nucleic Acids Res. 48: 606–612.
Dolinski K., Dwight S.S., Eppig J.T., Harris M.A. 2000. Gene ontology: tool for the unification of biology. Nat Gen. 25: 25–29.
Ewers C., Lübke-Becker A., Bethe A., Kießling S., Filter M., Wieler L.H. 2006. Virulence genotype of Pasteurella multocida strains isolated from different hosts with various disease status. Vet. Microbiol. 114: 304–317.
Harper M, Boyce D. 2017. The myriad properties of Pasteurella multocida lipopolysaccharide. Toxins, 9: 254.
Harper M., John M., Turni C., Edmunds M., St. Michael F., Adler B., et al. 2015. Development of a rapid multiplex PCR assay to genotype Pasteurella multocida strains by use of the lipopolysaccharide outer core biosynthesis locus. J. Clin. Microbiol. 53: 477–485.
Heddleston K.L., Gallagher J.E., Rebers P.A. 1972. Fowl cholera: gel diffusion precipitin test for serotyping Pasteurella multocida from avian species. Avian Dis. 925–936.
Henri C., Leekitcharoenphon P., Carleton H.A., Radomski N., Kaas R.S., Mariet J.F., et al. 2017. An assessment of different genomic approaches for inferring phylogeny of Listeria monocytogenes. Front. Microbiol. 2351.
Hotchkiss E.J., Hodgson J.C., Lainson F.A., Zadoks R.N. 2011. Multilocus sequence typing of a global collection of Pasteurella multocida isolates from cattle and other host species demonstrates niche association. BMC Microbiol. 11: 1–8.
Hui F.K. 2016. Boral–Bayesian ordination and regression analysis of multivariate abundance data in R. Methods Ecol. Evol. 7: 744–750.
Jackson R.W., Vinatzer B., Arnold D.L., Dorus S., Murillo J. 2011. The influence of the accessory genome on bacterial pathogen evolution. Mobile Genet. Elem. 1: 55–65.
Kaas R.S., Leekitcharoenphon P., Aarestrup F.M., Lund O. 2014. Solving the problem of comparing whole bacterial genomes across different sequencing platforms. PloS One, 9: e104984.
Kim J., Kim J.W., Oh S.I., So B., Kim W.I., Kim H.Y. 2019. Characterisation of Pasteurella multocida isolates from pigs with pneumonia in Korea. BMC Vet. Res. 15: 1–8.
Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., et al. 2009. The sequence alignment/map formatand SAMtools. Bioinformatics, 25: 2078–2079.
Li H., Durbin R. 2010. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics, 26: 589–595.
Liu B., Zheng D., Jin Q., Chen L., Yang J. 2019. VFDB 2019: VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res. 47: 687–692.
Liu S., Lin L., Yang H., Wu W., Guo L., Zhang Y., et al. 2021. Pasteurella multocida capsular: lipopolysaccharide types D:L6 and A:L3 remain to be the main epidemic genotypes of pigs in China. Anim. Dis. 1: 26.
Oliveira J.X.D., Morés M.A., Rebelatto R., Agnol A., Plieski C.L., Klein C.S., et al. 2015. Pasteurella multocida type A as the primary agent of pneumonia and septicaemia in pigs. Pesqui. Vet. Bras. 35: 716–724.
Page A.J., Cummins C.A., Hunt M., Wong V.K., Reuter S., Holden M.T., et al. 2015. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics, 31: 3691–3693.
Paz-Sánchez Y., Herráez P., Quesada-Canales Ó., Poveda C.G., Díaz-Delgado J., Quintana-Montesdeoca M.d.P., et al. 2021. Assessment of lung disease in finishing pigs at slaughter: pulmonary lesions and implications on productivity parameters. Animals, 3604.
Pearce M.E., Alikhan N.F., Dallman T.J., Zhou Z., Grant K., Maiden M.C. 2018. Comparative analysis of core genome MLST and SNP typing within a European Salmonella serovar Enteritidis outbreak.Int. J. Food. Microbiol. 274: 1–11.
Peng Z., Liang W., Wang F., Xu Z., Xie Z., Lian Z., et al. 2018. Genetic and phylogenetic characteristics of Pasteurella multocida isolates from different host species. Front. Microbiol. 9: 1408.
Peng Z., Wang X., Zhou R., Chen H., Wilson B.A., Wu B. 2019. Pasteurella multocida: genotypes and genomics. Microbiol. Mol. Biol. Rev. 83: e00014–e00019.
Peterson E., Kaur P. 2018. Antibiotic resistance mechanisms in bacteria: relationships between resistance determinants of antibiotic producers, environmental bacteria, and clinical pathogens. Front. Microbiol. 2928.
Portis E., Lindeman C., Johansen L., Stoltman G. 2013. Antimicrobial susceptibility of porcine Pasteurella multocida, Streptococcus suis, and Actinobacillus pleuropneumoniae from the United States and Canada, 2001 to 2010. J. Swine Health Prod. 21: 30–41.
Prajapati A., Chanda M.M., Yogisharadhya R., Parveen A., Ummer J., Dhayalan A., et al. 2020a. Comparative genetic diversity analysis based on virulence and repetitive genes profiling of circulating Pasteurella multocida isolates from animal hosts. Infect. Genet. Evol. 85: 104564.
Prajapati A., Chanda M.M., Dhayalan A., Yogisharadhya R., Chaudhary J.K., Mohanty N.N., Shivachandra S.B. 2020b. Variability in in vitro biofilm production and antimicrobial sensitivity pattern among Pasteurella multocida strains. Biofouling, 36: 938–950.
Prajapati A., Yogisharadhya R., Mohanty N.N., Mendem S.K., Nizamuddin A., Chanda M.M., Shivachandra S.B. 2022. Comparative genome analysis of Pasteurella multocida serogroup B:2 strains causing haemorrhagic septicaemia (HS) in bovines. Gene, 826: 146452.
Quinlan A.R., Hall I.M. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics, 26: 841–842.
Ramisetty B.C.M., Sudhakari P.A. 2019. Bacterial ‘grounded’ prophages: hotspots for genetic renovation and innovation. Front. Genet. 10: 65.
Ross R.F. 2006. Pasteurella multocida and its role in porcine pneumonia. Anim. Health. Res. Rev. 7: 13–29.
Sarangi L.N., Thomas P., Gupta S.K., Kumar S., Viswas K.N., Singh V.P. 2016. Molecular epidemiology of Pasteurella multocida circulating in India by multilocus sequence typing. Transbound. Emerg. Dis. 63: e286–e292.
Shivachandra S.B., Kumar A.A., Amaranath J., Joseph S., Srivastava S.K., Chaudhuri P. 2005. Cloning and characterization of tbpA gene encoding Transferrin binding protein (TbpA) from Pasteurella multocida B:2 (strain P52). Vet. Res. Commun. 29(6): 537–542..
Shivachandra S.B., Viswas K.N., Kumar A.A. 2011. A review of hemorrhagic septicemia in cattle and buffalo. Anim. Health. Res. Rev. 12: 67–82.
Shivachandra S.B., Yogisharadhya R., Kumar A., Mohanty N.N., Nagaleekar V.K. 2015. Recombinant transferrin binding protein A (TbpA) fragments of Pasteurella multocida serogroup B:2 provide variable protection following homologous challenge in mouse model. Res. Vet. Sci. 98(1): 1–6.
Shivachandra S.B., Chanda M.M., Hiremath J., Yogisharadhya R., Mohanty N.N., Hemadri D. 2017. Molecular diagnostic approaches for haemorrhagic septicaemia (HS): a review. Ind. J. Comp. Microbiol. Immunol. Infect. Dis. 38(2): 51–65.
Shyam S., Tamuly S., Borah P., Sharma R.K. 2020. Protective efficacy of calcium phosphate nanoparticle adsorbed bivalent subunit vaccine of Pasteurella multocida against homologous challenge in mice. bioRxiv.
Siddaramappa S. 2021. Comparative genomics of the Pasteurella multocida toxin. Genome, 64: 679–692.
Smith E., Miller E., Aguayo J.M., Figueroa C.F., Nezworski J., Studniski M., et al. 2021. Genomic diversity and molecular epidemiology of Pasteurella multocida. PLoS One, 16: e0249138.
Tatusova T., Di Cuccio M., Badretdin A., Chetvernin V., Nawrocki E. P., Zaslavsky L., et al. 2016. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 44: 6614–6624.
Tsang A.K.L., Lee H. H., Yiu S. M., Lau S. K. P., Woo P.C.Y. 2017. Failure of phylogeny inferred from multilocus sequence typing to represent bacterial phylogeny. Sci. Rep. 7: 4536.
Ujvári B., Szeredi L., Pertl L., Tóth G., Erdélyi K., Jánosi S., et al. 2015. First detection of Pasteurella multocida type B:2 in Hungary associated with systemic pasteurellosis in backyard pigs. Acta Vet. Hung. 63: 141–156.
Wilson B.A., Ho M. 2013. Pasteurella multocida: from zoonosis to cellular microbiology. Clin. Microbiol. Rev. 26: 631–655.
Yakkala H., Samantarrai D., Gribskov M., Siddavattam D. 2019. Comparative genome analysis reveals niche-specific genome expansion in Acinetobacter baumannii strains. PLoS One, 14: e0218204.
Yoon S.H., Ha S.M., Kwon S., Lim J., Kim Y., Seo H., Chun J. 2017. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int. J. Sys. Evol. Microbiol. 67: 1613.

Supplementary material

Supplementary Material 1 (DOCX / 20.7 KB).
Supplementary Material 2 (DOCX / 16.0 KB).
Supplementary Material 3 (DOCX / 16.5 KB).
Supplementary Material 4 (DOCX / 12.8 KB).
Supplementary Material 5 (DOCX / 20.5 KB).
Supplementary Material 6 (CSV / 2.58 KB).
Supplementary Material 7 (CSV / 2.43 KB).
Supplementary Material 8 (XLSX / 18.2 KB).
Supplementary Material 9 (TIF / 199 KB).
Supplementary Material 10 (TIF / 189 KB).
Supplementary Material 11 (TIF / 259 KB).

Information & Authors

Information

Published In

cover image Genome
Genome
Volume 67Number 1January 2024
Pages: 13 - 23

History

Received: 31 March 2023
Accepted: 22 August 2023
Accepted manuscript online: 28 August 2023
Version of record online: 28 September 2023

Data Availability Statement

Genome sequences of NIVEDIPm17 and NIVEDIPm36 have been deposited in the National Center for Biotechnology Information (NCBI) Sequence genome submission portal and have been assigned the accession ID of JAKNTU00000000 and JAKNTV000000000, respectively. Further, raw Illumina sequence read data have been deposited in the NCBI sequence read archive [SRA (https://www.ncbi.nlm.nih.gov/sra)] under the accession numbers PRJNA804361 and PRJNA804365, respectively.

Permissions

Request permissions for this article.

Key Words

  1. capsular serogroups
  2. genome analysis
  3. Pasteurella multocida
  4. porcine
  5. vaccine

Authors

Affiliations

ICAR – National Institute of Veterinary Epidemiology and Disease Informatics (NIVEDI), Bengaluru 560064, Karnataka, India
Author Contributions: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Visualization, and Writing – original draft.
ICAR – National Institute of Veterinary Epidemiology and Disease Informatics (NIVEDI), Bengaluru 560064, Karnataka, India
Author Contributions: Investigation, Methodology, Resources, and Writing – review & editing.
CCS – National Institute of Animal Health (NIAH), Baghpat 250609, Uttar Pradesh, India
Author Contributions: Investigation and Resources.
Suresh Kumar Mendem
ICAR – National Institute of Veterinary Epidemiology and Disease Informatics (NIVEDI), Bengaluru 560064, Karnataka, India
Author Contributions: Data curation, Methodology, and Software.
Mohammed Mudassar Chanda https://orcid.org/0000-0002-5727-8658
ICAR – National Institute of Veterinary Epidemiology and Disease Informatics (NIVEDI), Bengaluru 560064, Karnataka, India
Author Contributions: Formal analysis, Methodology, Software, and Writing – review & editing.
Shivakumara Siddaramappa
Institute of Bioinformatics and Applied Biotechnology (IBAB), Bengaluru 560100, Karnataka, India
Author Contributions: Methodology, Validation, and Writing – review & editing.
ICAR – National Institute of Veterinary Epidemiology and Disease Informatics (NIVEDI), Bengaluru 560064, Karnataka, India
Author Contributions: Funding acquisition, Project administration, Resources, Supervision, and Writing – review & editing.

Author Contributions

Conceptualization: AP
Data curation: AP, SKM
Formal analysis: AP, MMC
Funding acquisition: SBS
Investigation: AP, RY, NNM
Methodology: AP, RY, SKM, MMC, SS
Project administration: SBS
Resources: RY, NNM, SBS
Software: SKM, MMC
Supervision: SBS
Validation: SS
Visualization: AP
Writing – original draft: AP
Writing – review & editing: RY, MMC, SS, SBS

Competing Interests

The authors declare no competing interests.

Funding Information

This study was a part of doctoral research carried out by AP under the institute project (Code: IXX12176) entitled “Epidemiology of haemorrhagic septicaemia (HS) in India” granted to SBS.

Metrics & Citations

Metrics

Other Metrics

Citations

Cite As

Export Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

Cited by

1. PMCNA_RS00975 activates NF-κB and ERK1/2 through TLR2 and contributes to the virulence of Pasteurella multocida
2. Development of a Triplex qPCR Assay Based on the TaqMan Probe for the Detection of Haemophilus parasuis, Streptococcus suis Serotype 2 and Pasteurella multocida
3. Pathogenicity and Genomic Characteristics Analysis of Pasteurella multocida Serotype A Isolated from Argali Hybrid Sheep

View Options

Login options

Check if you access through your login credentials or your institution to get full access on this article.

Subscribe

Click on the button below to subscribe to Genome

Purchase options

Purchase this article to get full access to it.

Restore your content access

Enter your email address to restore your content access:

Note: This functionality works only for purchases done as a guest. If you already have an account, log in to access the content to which you are entitled.

View options

PDF

View PDF

Full Text

View Full Text

Figures

Tables

Media

Share Options

Share

Share the article link

Share on social media