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Comparative phylogenomics of Trueperella pyogenes reveals host-based distinction of strains

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Abstract

Trueperella pyogenes, an opportunistic pathogen causes various ailments in different animals. Different strains from different animals have distinct characters phenotypically and genotypically. Hence understanding the strains in a particular geographical location helps in framing the preventive measures. Comparative genomics of all the available T. pyogenes genome in the NCBI was conducted to understand the relatedness among strains. Whole genome phylogeny showed host associated clustering of strains recovered from swine lungs. Core genome phylogeny also showed host associated clustering mimicking whole genome phylogeny results. MLST analysis showed that there was higher diversity among cattle strains. Multidimensional scaling revealed five swine clusters, two cattle and buffalo clusters. Pangenome analysis also showed that T. pyogenes had an open genome with 57.09% accessory genome. Host specific genes were identified by pangenome analysis, and (R)-citramalate synthase was specific for swine strains of Asian origin. Host specifc genes identified by pangenome analysis can be exploited for developing a molecular assay to specifically identify the strains. The study shows that MLST having higher discriminatory power can be used as an epidemiological tool for strain discrimination of T. pyogenes.

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The data used to support the findings of this study is included in the article. Supporting data are included as supportive tables.

References

  • Ashrafi Tamai I, Mohammadzadeh A, Zahraei Salehi T, Mahmoodi P (2018) Genomic characterisation, detection of genes encoding virulence factors and evaluation of antibiotic resistance of Trueperella pyogenes isolated from cattle with clinical metritis. Antonie Van Leeuwenhoek 111:2441–2453

    Article  CAS  PubMed  Google Scholar 

  • Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA, Bentley SD, Parkhill J, Harris SR (2015) Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 43:e15

    Article  PubMed  Google Scholar 

  • Diene SM, Merhej V, Henry M, El Filali A, Roux V, Robert C, Azza S, Gavory F, Barbe V, La Scola B, Raoult D, Rolain JM (2013) The rhizome of the multidrug-resistant Enterobacter aerogenes genome reveals how new “Killer Bugs” are created because of a sympatric lifestyle. Mol Biol Evol 30:369–383

    Article  CAS  PubMed  Google Scholar 

  • Fujimoto H, Shimoji N, Sunagawa T, Kubozono K, Nakajima T, Chuma C (2020) Differences in phenotypic and genetic characteristics of Trueperella pyogenes detected in slaughtered cattle and pigs with septicemia. J Vet Med Sci 82:626–631. https://doi.org/10.1292/jvms.19-0370

    Article  PubMed  PubMed Central  Google Scholar 

  • Grim CJ, Kotewicz ML, Power KA, Gopinath G, Franco AA, Jarvis KG, Yan QQ, Jackson SA, Sathyamoorthy V, Hu L, Pagotto F, Iversen C, Lehner A, Stephan R, Fanning S, Tall BD (2013) Pan-genome analysis of the emerging foodborne pathogen Cronobacter spp. suggests a species-level bidirectional divergence driven by niche adaptation. BMC Genomics 14:366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Juhas M, Van der Meer JR, Gaillard M, Harding RM, Hood D, Crook DW (2009) Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev 33:376–393. https://doi.org/10.1111/j.1574-6976.2008.00136.x

    Article  CAS  PubMed  Google Scholar 

  • Karthik K, Anbazhagan S, Thomas P, Ananda Chitra M, Senthilkumar TMA, Sridhar R, Dhinakar Raj G (2021) Genome sequencing and comparative Genomics of Indian isolates of Brucella melitensis. Front Microbiol 12:698069. https://doi.org/10.3389/fmicb.2021.698069

    Article  PubMed  PubMed Central  Google Scholar 

  • Karthik K, Anbazhagan S, Chitra MA, Bharathi R, Venkataramanan R, Manobhavan M, Sundaram SM, Sridhar R (2022) Comparative genomics of Trueperella pyogenes available in the genome database reveals multidrug resistance genomic islands. J Global Antimicrob Resist S2213-7165(22)00225-9. https://doi.org/10.1016/j.jgar.2022.09.011

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Bork P (2021) Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49:W293–W296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marschall T, Marz M, Abeel T, Dijkstra L, Dutilh BE, Ghaffaari A, Kersey P, Kloosterman WP, Mäkinen V, Novak AM (2018) The computational Pan-Genomics Consortium. Computational pan-genomics: Status, promises and challenges. Brief Bioinform 19:118–135

    CAS  Google Scholar 

  • Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R (2005) The microbial pan-genome. Curr Opin Genet Dev 5:589–594

    Article  Google Scholar 

  • Nagib S, Glaeser SP, Eisenberg T, Sammra O, Lämmler C, Kämpfer P, Schauerte N, Geiger C, Kaim U, Prenger-Berninghoff E, Becker A, Abdulmawjood A (2017) Fatal infection in three Grey Slender Lorises (Loris lydekkerianus nordicus) caused by clonally related Trueperella pyogenes. BMC Vet Res 13:273. https://doi.org/10.1186/s12917-017-1171-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nourdin-Galindo G, Sánchez P, Molina CF, Espinoza-Rojas DA, Oliver C, Ruiz P, Vargas-Chacoff L, Cárcamo JG, Figueroa JE, Mancilla M, Maracaja-Coutinho V, Yañez AJ (2017) Comparative pan-genome analysis of Piscirickettsia salmonis reveals genomic divergences within genogroups. Front Cell Infect Microbiol 7:459. https://doi.org/10.3389/fcimb.2017.00459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rasko DA, Rosovitz MJ, Myers GS, Mongodin EF, Fricke WF, Gajer P, Crabtree J, Sebaihia M, Thomson NR, Chaudhuri R, Henderson IR (2008) The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 190:6881–6893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rogovskyy AS, Lawhon S, Kuczmanski K, Gillis DC, Wu J, Hurley H, Rogovska YV, Konganti K, Yang CY, Duncan K (2018) Phenotypic and genotypic characteristics of Trueperella pyogenes isolated from ruminants. J Vet Diagn Invest 30:348–353. https://doi.org/10.1177/1040638718762479

    Article  PubMed  PubMed Central  Google Scholar 

  • Rzewuska M, Kwiecień E, Chrobak-Chmiel D, Kizerwetter-Świda M, Stefańska I, Gieryńska M (2019) Pathogenicity and virulence of Trueperella pyogenes: a review. Int J Mol Sci 20:2737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seemann T (2019) snp-dists. GitHub repository. GitHub. Retrieved from https://github.com/tseemann/snp-dists

  • Silva E, Gaivão M, Leitão S, Jost BH, Carneiro C, Vilela CL, Lopes da Costa L, Mateus L (2008) Genomic characterization of Arcanobacterium pyogenes isolates recovered from the uterus of dairy cows with normal puerperium or clinical metritis. Vet Microbiol 132:111–118

    Article  CAS  PubMed  Google Scholar 

  • Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS, Deboy RT, Davidsen TM, Mora M, Scarselli M, Margarit /Dodson RJ, Rosovitz MJ, Sullivan SA, Daugherty SC, Haft DH, Selengut J, Gwinn ML, Zhou L, Zafar N, Khouri H, Radune D, Dimitrov G, Watkins K, O’Connor KJ, Smith S, Utterback TR, White O, Rubens CE, Grandi G, Madoff LC, Kasper DL, Telford JL, Wessels MR, Rappuoli R, Fraser CM (2005) Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome.” Proc Natl Acad Sci 102:13950–13955. https://doi.org/10.1073/pnas.0506758102

  • Tomasini N, Lauthier JJ, Llewellyn MS, Diosque P (2013) MLSTest: novel software for multi-locus sequence data analysis in eukaryotic organisms. Infect Genet Evol 20:188–196

    Article  CAS  PubMed  Google Scholar 

  • Tonkin-Hill G, MacAlasdair N, Ruis C, Weimann A, Horesh G, Lees JA, Gladstone RA, Lo S, Beaudoin C, Floto RA, Frost SD (2020) Producing polished prokaryotic pangenomes with the Panaroo pipeline. Genome Biol 21:1–21

    Article  Google Scholar 

  • Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ (2016) IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 44:W232–W235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Jia X, Yang J, Ling Y, Zhang Z, Yu J, Wu J, Xiao J (2014) PanGP: a tool for quickly analyzing bacterial pan-genome profile. Bioinformatics 30:1297–1299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors are thankful to Tamil Nadu Veterinary and Animal Sciences University for the facilities provided for carrying out the work.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Authors and Affiliations

  1. Central University Laboratory, Tamil Nadu Veterinary and Animal Sciences University, Chennai, Tamil Nadu, 600051, India

    Kumaragurubaran Karthik, Murugesan Ananda Chitra & Ramaswamy Sridhar

  2. Department of Veterinary Microbiology, Veterinary College and Research Institute, Tamil Nadu Veterinary and Animal Sciences University, Udumalpet, Tamil Nadu, 642126, India

    Kumaragurubaran Karthik

  3. ICMR-National Animal Resource Facility for Biomedical Research, Hyderabad, 500078, India

    Subbaiyan Anbazhagan

Authors
  1. Kumaragurubaran Karthik
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  2. Subbaiyan Anbazhagan
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  4. Ramaswamy Sridhar
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Contributions

All authors contributed to the study conception and design. Kumaragurubaran Karthik: Conceptualization, isolation of T. pyogenes from the samples, formal analysis, writing original draft; Subbaiyan Anbazhagan: data curation, software analysis, updating original manuscript; Murugesan Ananda Chitra: Data curation, reviewing and editing of the draft; Ramaswamy Sridhar: Fund acquisition and administration.

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Correspondence to Kumaragurubaran Karthik.

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Karthik, K., Anbazhagan, S., Chitra, M.A. et al. Comparative phylogenomics of Trueperella pyogenes reveals host-based distinction of strains. Antonie van Leeuwenhoek 116, 343–351 (2023). https://doi.org/10.1007/s10482-022-01806-9

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  • DOI: https://doi.org/10.1007/s10482-022-01806-9

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