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Microbiology spectrum2022; 10(1); e0076421; doi: 10.1128/spectrum.00764-21

Differences in the Accessory Genomes and Methylomes of Strains of Streptococcus equi subsp. equi and of Streptococcus equi subsp. zooepidemicus Obtained from the Respiratory Tract of Horses from Texas.

Abstract: Streptococcus equi subsp. (SEE) is a host-restricted equine pathogen considered to have evolved from Streptococcus equi subsp. (SEZ). SEZ is promiscuous in host range and is commonly recovered from horses as a commensal. Comparison of a single strain each of SEE and SEZ using whole-genome sequencing, supplemented by PCR of selected genes in additional SEE and SEZ strains, was used to characterize the evolution of SEE. But the known genetic variability of SEZ warrants comparison of the whole genomes of multiple SEE and SEZ strains. To fill this knowledge gap, we utilized whole-genome sequencing to characterize the accessory genome elements (AGEs; i.e., elements present in some SEE strains but absent in SEZ or vice versa) and methylomes of 50 SEE and 50 SEZ isolates from Texas. Consistent with previous findings, AGEs consistently found in all SEE isolates were primarily from mobile genetic elements that might contribute to host restriction or pathogenesis of SEE. Fewer AGEs were identified in SEZ because of the greater genomic variability among these isolates. The global methylation patterns of SEE isolates were more consistent than those of the SEZ isolates. Among homologous genes of SEE and SEZ, differential methylation was identified only in genes of SEE encoding proteins with functions of quorum sensing, exopeptidase activity, and transitional metal ion binding. Our results indicate that effects of genetic mobile elements in SEE and differential methylation of genes shared by SEE and SEZ might contribute to the host specificity of SEE. Strangles, caused by the host-specific bacterium Streptococcus equi subsp. (SEE), is the most commonly diagnosed infectious disease of horses worldwide. Its ancestor, Streptococcus equi subsp. (SEZ), is frequently isolated from a wide array of hosts, including horses and humans. A comparison of the genomes of a single strain of SEE and SEZ has been reported, but sequencing of further isolates has revealed variability among SEZ strains. Thus, the importance of this study is that it characterizes genomic and methylomic differences of multiple SEE and SEZ isolates from a common geographic region (, Texas). Our results affirm many of the previously described differences between the genomes of SEE and SEZ, including the role of mobile genetic elements in contributing to host restriction. We also provide the first characterization of the global methylome of Streptococcus equi and evidence that differential methylation might contribute to the host restriction of SEE.
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Publication Date: 2022-01-12 PubMed ID: 35019696PubMed Central: PMC8754150DOI: 10.1128/spectrum.00764-21Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research investigates the genetic and epigenetic differences between two pathogenic subspecies of Streptococcus equi bacteria that are found in horses, with the aim to understand how specific strains have evolved to specialize in particular host species.

Research Objective

  • The goal of this research was to understand more clearly how the streptococcus equi subspecies equi (SEE) bacteria have evolved to limit their infection host to only horses, whereas the subspecies zooepidemicus (SEZ) can infect a broader range of hosts.
  • To achieve this, researchers compared the accessory genome elements (AGEs) and the methylation patterns – components of the total genome – of 50 SEE and SEZ bacterial isolates taken from horses in Texas. AGEs are parts of the genome which may be present in certain strains but not in others, and could offer insights into genetic adaptations.

Findings

  • They found that the AGEs consistently found in all SEE isolates came from mobile genetic elements which could contribute to host restriction or pathogenesis of SEE. However, the SEZ subspecies exhibited fewer AGEs, potentially due to increased genetic variability among these isolates.
  • The global methylation patterns of SEE isolates were more consistent than those of SEZ isolates. Also, in genes common to both subspecies, only SEE showed differential methylation specifically in genes encoding proteins with functions of quorum sensing, exoprotease activity, and transitional metal ion binding.

Conclusion

  • This study concluded that the effects of mobile genetic elements and differential methylation might be key factors contributing to the host specificity of the SEE bacteria, confirming some previous findings and presenting novel insights.
  • This research not only affirmed many previously described differences between the genomes of SEE and SEZ subspecies but also demonstrated for the first time the differential DNA methylation patterns of Streptococcus equi genomes, suggesting their potential role in determining host specificity of the bacteria.

Cite This Article

APA
Morris ERA, Wu J, Bordin AI, Lawhon SD, Cohen ND. (2022). Differences in the Accessory Genomes and Methylomes of Strains of Streptococcus equi subsp. equi and of Streptococcus equi subsp. zooepidemicus Obtained from the Respiratory Tract of Horses from Texas. Microbiol Spectr, 10(1), e0076421. https://doi.org/10.1128/spectrum.00764-21

Publication

Microbiology spectrum
ISSN: 2165-0497
NlmUniqueID: 101634614
Country: United States
Language: English
Volume: 10
Issue: 1
Pages: e0076421
PII: e00764-21

Researcher Affiliations

Morris, Ellen Ruth A
  • Department of Large Animal Clinical Sciences, College of Veterinary Medicine & Biomedical Sciences, Texas A&M University, College Station, Texas, USA.
Wu, Jing
  • Department of Veterinary Pathobiology, College of Veterinary Medicine & Biomedical Sciences, Texas A&M University, College Station, Texas, USA.
Bordin, Angela I
  • Department of Large Animal Clinical Sciences, College of Veterinary Medicine & Biomedical Sciences, Texas A&M University, College Station, Texas, USA.
Lawhon, Sara D
  • Department of Veterinary Pathobiology, College of Veterinary Medicine & Biomedical Sciences, Texas A&M University, College Station, Texas, USA.
Cohen, Noah D
  • Department of Large Animal Clinical Sciences, College of Veterinary Medicine & Biomedical Sciences, Texas A&M University, College Station, Texas, USA.

MeSH Terms

  • Animals
  • DNA Methylation
  • Epigenome
  • Genetic Variation
  • Genome, Bacterial
  • Horse Diseases / microbiology
  • Horses
  • Respiratory System / microbiology
  • Streptococcal Infections / microbiology
  • Streptococcal Infections / veterinary
  • Streptococcus / classification
  • Streptococcus / genetics
  • Streptococcus / isolation & purification
  • Streptococcus equi / classification
  • Streptococcus equi / genetics
  • Streptococcus equi / isolation & purification
  • Texas

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 64 references
  1. Waller AS, Paillot R, Timoney JF. Streptococcus equi: a pathogen restricted to one host.. J Med Microbiol 2011 Sep;60(Pt 9):1231-1240.
    doi: 10.1099/jmm.0.028233-0pubmed: 21757503google scholar: lookup
  2. Boyle AG, Timoney JF, Newton JR, Hines MT, Waller AS, Buchanan BR. Streptococcus equi Infections in Horses: Guidelines for Treatment, Control, and Prevention of Strangles-Revised Consensus Statement.. J Vet Intern Med 2018 Mar;32(2):633-647.
    doi: 10.1111/jvim.15043pmc: PMC5867011pubmed: 29424487google scholar: lookup
  3. Paillot R, Lopez-Alvarez MR, Newton JR, Waller AS. Strangles: A modern clinical view from the 17th century.. Equine Vet J 2017 Mar;49(2):141-145.
    doi: 10.1111/evj.12659pubmed: 28177153google scholar: lookup
  4. Sweeney CR, Timoney JF, Newton JR, Hines MT. Streptococcus equi infections in horses: guidelines for treatment, control, and prevention of strangles.. J Vet Intern Med 2005 Jan-Feb;19(1):123-34.
    doi: 10.1111/j.1939-1676.2005.tb02671.xpubmed: 15715061google scholar: lookup
  5. Slater JD. Strangles, bastard strangles, vives and glanders: archaeological relics in a genomic age.. Equine Vet J 2003 Mar;35(2):118-20.
    doi: 10.2746/042516403776114252pubmed: 12638785google scholar: lookup
  6. Holden MT, Heather Z, Paillot R, Steward KF, Webb K, Ainslie F, Jourdan T, Bason NC, Holroyd NE, Mungall K, Quail MA, Sanders M, Simmonds M, Willey D, Brooks K, Aanensen DM, Spratt BG, Jolley KA, Maiden MC, Kehoe M, Chanter N, Bentley SD, Robinson C, Maskell DJ, Parkhill J, Waller AS. Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens.. PLoS Pathog 2009 Mar;5(3):e1000346.
    doi: 10.1371/journal.ppat.1000346pmc: PMC2654543pubmed: 19325880google scholar: lookup
  7. Webb K, Jolley KA, Mitchell Z, Robinson C, Newton JR, Maiden MCJ, Waller A. Development of an unambiguous and discriminatory multilocus sequence typing scheme for the Streptococcus zooepidemicus group.. Microbiology (Reading) 2008 Oct;154(Pt 10):3016-3024.
    doi: 10.1099/mic.0.2008/018911-0pubmed: 18832307google scholar: lookup
  8. Harris SR, Robinson C, Steward KF, Webb KS, Paillot R, Parkhill J, Holden MT, Waller AS. Genome specialization and decay of the strangles pathogen, Streptococcus equi, is driven by persistent infection.. Genome Res 2015 Sep;25(9):1360-71.
    doi: 10.1101/gr.189803.115pmc: PMC4561494pubmed: 26160165google scholar: lookup
  9. Newton JR, Laxton R, Wood JL, Chanter N. Molecular epidemiology of Streptococcus zooepidemicus infection in naturally occurring equine respiratory disease.. Vet J 2008 Mar;175(3):338-45.
    doi: 10.1016/j.tvjl.2007.02.018pubmed: 17433734google scholar: lookup
  10. Timoney JF. The pathogenic equine streptococci.. Vet Res 2004 Jul-Aug;35(4):397-409.
    doi: 10.1051/vetres:2004025pubmed: 15236673google scholar: lookup
  11. Lindahl SB, Aspán A, Båverud V, Paillot R, Pringle J, Rash NL, Söderlund R, Waller AS. Outbreak of upper respiratory disease in horses caused by Streptococcus equi subsp. zooepidemicus ST-24.. Vet Microbiol 2013 Sep 27;166(1-2):281-5.
    doi: 10.1016/j.vetmic.2013.05.006pubmed: 23773239google scholar: lookup
  12. Björnsdóttir S, Harris SR, Svansson V, Gunnarsson E, Sigurðardóttir ÓG, Gammeljord K, Steward KF, Newton JR, Robinson C, Charbonneau ARL, Parkhill J, Holden MTG, Waller AS. Genomic Dissection of an Icelandic Epidemic of Respiratory Disease in Horses and Associated Zoonotic Cases.. mBio 2017 Aug 1;8(4).
    doi: 10.1128/mBio.00826-17pmc: PMC5539424pubmed: 28765219google scholar: lookup
  13. Pelkonen S, Lindahl SB, Suomala P, Karhukorpi J, Vuorinen S, Koivula I, Väisänen T, Pentikäinen J, Autio T, Tuuminen T. Transmission of Streptococcus equi subspecies zooepidemicus infection from horses to humans.. Emerg Infect Dis 2013 Jul;19(7):1041-8.
    doi: 10.3201/eid1907.121365pmc: PMC3713971pubmed: 23777752google scholar: lookup
  14. Chen X, Resende-De-Macedo N, Sitthicharoenchai P, Sahin O, Burrough E, Clavijo M, Derscheid R, Schwartz K, Lantz K, Robbe-Austerman S, Main R, Li G. Genetic characterization of Streptococcus equi subspecies zooepidemicus associated with high swine mortality in the United States.. Transbound Emerg Dis 2020 Nov;67(6):2797-2808.
    doi: 10.1111/tbed.13645pubmed: 32460392google scholar: lookup
  15. Byun JW, Yoon SS, Woo GH, Jung BY, Joo YS. An outbreak of fatal hemorrhagic pneumonia caused by Streptococcus equi subsp. zooepidemicus in shelter dogs.. J Vet Sci 2009 Sep;10(3):269-71.
    doi: 10.4142/jvs.2009.10.3.269pmc: PMC2801124pubmed: 19687630google scholar: lookup
  16. Las Heras A, Vela AI, Fernández E, Legaz E, Domínguez L, Fernández-Garayzábal JF. Unusual outbreak of clinical mastitis in dairy sheep caused by Streptococcus equi subsp. zooepidemicus.. J Clin Microbiol 2002 Mar;40(3):1106-8.
    doi: 10.1128/JCM.40.3.1106-1108.2002pmc: PMC120234pubmed: 11880454google scholar: lookup
  17. Blum S, Elad D, Zukin N, Lysnyansky I, Weisblith L, Perl S, Netanel O, David D. Outbreak of Streptococcus equi subsp. zooepidemicus infections in cats.. Vet Microbiol 2010 Jul 29;144(1-2):236-9.
    doi: 10.1016/j.vetmic.2009.12.040pmc: PMC7126194pubmed: 20106608google scholar: lookup
  18. Preziuso S, Moriconi M, Cuteri V. Genetic diversity of Streptococcus equi subsp. zooepidemicus isolated from horses.. Comp Immunol Microbiol Infect Dis 2019 Aug;65:7-13.
    doi: 10.1016/j.cimid.2019.03.012pubmed: 31300129google scholar: lookup
  19. Ozer EA, Allen JP, Hauser AR. Characterization of the core and accessory genomes of Pseudomonas aeruginosa using bioinformatic tools Spine and AGEnt.. BMC Genomics 2014 Aug 29;15(1):737.
    doi: 10.1186/1471-2164-15-737pmc: PMC4155085pubmed: 25168460google scholar: lookup
  20. Gao XY, Zhi XY, Li HW, Klenk HP, Li WJ. Comparative genomics of the bacterial genus Streptococcus illuminates evolutionary implications of species groups.. PLoS One 2014;9(6):e101229.
    doi: 10.1371/journal.pone.0101229pmc: PMC4076318pubmed: 24977706google scholar: lookup
  21. Flusberg BA, Webster DR, Lee JH, Travers KJ, Olivares EC, Clark TA, Korlach J, Turner SW. Direct detection of DNA methylation during single-molecule, real-time sequencing.. Nat Methods 2010 Jun;7(6):461-5.
    doi: 10.1038/nmeth.1459pmc: PMC2879396pubmed: 20453866google scholar: lookup
  22. Blow MJ, Clark TA, Daum CG, Deutschbauer AM, Fomenkov A, Fries R, Froula J, Kang DD, Malmstrom RR, Morgan RD, Posfai J, Singh K, Visel A, Wetmore K, Zhao Z, Rubin EM, Korlach J, Pennacchio LA, Roberts RJ. The Epigenomic Landscape of Prokaryotes.. PLoS Genet 2016 Feb;12(2):e1005854.
    doi: 10.1371/journal.pgen.1005854pmc: PMC4752239pubmed: 26870957google scholar: lookup
  23. Sánchez-Romero MA, Cota I, Casadesús J. DNA methylation in bacteria: from the methyl group to the methylome.. Curr Opin Microbiol 2015 Jun;25:9-16.
    doi: 10.1016/j.mib.2015.03.004pubmed: 25818841google scholar: lookup
  24. Nye TM, Jacob KM, Holley EK, Nevarez JM, Dawid S, Simmons LA, Watson ME Jr. DNA methylation from a Type I restriction modification system influences gene expression and virulence in Streptococcus pyogenes.. PLoS Pathog 2019 Jun;15(6):e1007841.
    doi: 10.1371/journal.ppat.1007841pmc: PMC6597129pubmed: 31206562google scholar: lookup
  25. Gomez-Gonzalez PJ, Andreu N, Phelan JE, de Sessions PF, Glynn JR, Crampin AC, Campino S, Butcher PD, Hibberd ML, Clark TG. An integrated whole genome analysis of Mycobacterium tuberculosis reveals insights into relationship between its genome, transcriptome and methylome.. Sci Rep 2019 Mar 26;9(1):5204.
    doi: 10.1038/s41598-019-41692-2pmc: PMC6435705pubmed: 30914757google scholar: lookup
  26. Casselli T, Tourand Y, Scheidegger A, Arnold WK, Proulx A, Stevenson B, Brissette CA. DNA Methylation by Restriction Modification Systems Affects the Global Transcriptome Profile in Borrelia burgdorferi.. J Bacteriol 2018 Dec 15;200(24).
    doi: 10.1128/JB.00395-18pmc: PMC6256022pubmed: 30249703google scholar: lookup
  27. Furuta Y, Kobayashi I. Mobility of DNA sequence recognition domains in DNA methyltransferases suggests epigenetics-driven adaptive evolution.. Mob Genet Elements 2012 Nov 1;2(6):292-296.
    doi: 10.4161/mge.23371pmc: PMC3575425pubmed: 23481556google scholar: lookup
  28. Heather Z, Holden MT, Steward KF, Parkhill J, Song L, Challis GL, Robinson C, Davis-Poynter N, Waller AS. A novel streptococcal integrative conjugative element involved in iron acquisition.. Mol Microbiol 2008 Dec;70(5):1274-92.
    doi: 10.1111/j.1365-2958.2008.06481.xpmc: PMC3672683pubmed: 18990191google scholar: lookup
  29. Paillot R, Robinson C, Steward K, Wright N, Jourdan T, Butcher N, Heather Z, Waller AS. Contribution of each of four Superantigens to Streptococcus equi-induced mitogenicity, gamma interferon synthesis, and immunity.. Infect Immun 2010 Apr;78(4):1728-39.
    doi: 10.1128/IAI.01079-09pmc: PMC2849420pubmed: 20123710google scholar: lookup
  30. Poindexter NJ, Schlievert PM. Suppression of immunoglobulin-secreting cells from human peripheral blood by toxic-shock-syndrome toxin-1.. J Infect Dis 1986 Apr;153(4):772-9.
    doi: 10.1093/infdis/153.4.772pubmed: 3512737google scholar: lookup
  31. Bohach GA, Fast DJ, Nelson RD, Schlievert PM. Staphylococcal and streptococcal pyrogenic toxins involved in toxic shock syndrome and related illnesses.. Crit Rev Microbiol 1990;17(4):251-72.
    doi: 10.3109/10408419009105728pubmed: 2206394google scholar: lookup
  32. Roberts RJ, Vincze T, Posfai J, Macelis D. REBASE--a database for DNA restriction and modification: enzymes, genes and genomes.. Nucleic Acids Res 2015 Jan;43(Database issue):D298-9.
    doi: 10.1093/nar/gk၆pmc: PMC4383893pubmed: 25378308google scholar: lookup
  33. Brachmann CB, Sherman JM, Devine SE, Cameron EE, Pillus L, Boeke JD. The SIR2 gene family, conserved from bacteria to humans, functions in silencing, cell cycle progression, and chromosome stability.. Genes Dev 1995 Dec 1;9(23):2888-902.
    doi: 10.1101/gad.9.23.2888pubmed: 7498786google scholar: lookup
  34. Okumura K, Shimomura Y, Murayama SY, Yagi J, Ubukata K, Kirikae T, Miyoshi-Akiyama T. Evolutionary paths of streptococcal and staphylococcal superantigens.. BMC Genomics 2012 Aug 17;13:404.
    doi: 10.1186/1471-2164-13-404pmc: PMC3538662pubmed: 22900646google scholar: lookup
  35. Fast DJ, Schlievert PM, Nelson RD. Nonpurulent response to toxic shock syndrome toxin 1-producing Staphylococcus aureus. Relationship to toxin-stimulated production of tumor necrosis factor.. J Immunol 1988 Feb 1;140(3):949-53.
    pubmed: 3339245
  36. Spaulding AR, Salgado-Pabón W, Kohler PL, Horswill AR, Leung DY, Schlievert PM. Staphylococcal and streptococcal superantigen exotoxins.. Clin Microbiol Rev 2013 Jul;26(3):422-47.
    doi: 10.1128/CMR.00104-12pmc: PMC3719495pubmed: 23824366google scholar: lookup
  37. Jorm LR, Love DN, Bailey GD, McKay GM, Briscoe DA. Genetic structure of populations of beta-haemolytic Lancefield group C streptococci from horses and their association with disease.. Res Vet Sci 1994 Nov;57(3):292-9.
    doi: 10.1016/0034-5288(94)90120-1pubmed: 7871247google scholar: lookup
  38. Grant ST, Efstratiou A, Chanter N. Laboratory diagnosis of strangles and the isolation of atypical Streptococcus equi.. Vet Rec 1993 Aug 28;133(9):215-6.
    doi: 10.1136/vr.133.9.215pubmed: 8236725google scholar: lookup
  39. Morris ERA, Hillhouse AE, Konganti K, Wu J, Lawhon SD, Bordin AI, Cohen ND. Comparison of whole genome sequences of Streptococcus equi subsp. equi from an outbreak in Texas with isolates from within the region, Kentucky, USA, and other countries.. Vet Microbiol 2020 Apr;243:108638.
    doi: 10.1016/j.vetmic.2020.108638pubmed: 32273017google scholar: lookup
  40. Kelly C, Bugg M, Robinson C, Mitchell Z, Davis-Poynter N, Newton JR, Jolley KA, Maiden MC, Waller AS. Sequence variation of the SeM gene of Streptococcus equi allows discrimination of the source of strangles outbreaks.. J Clin Microbiol 2006 Feb;44(2):480-6.
    doi: 10.1128/JCM.44.2.480-486.2006pmc: PMC1392674pubmed: 16455902google scholar: lookup
  41. Hoch JA. Two-component and phosphorelay signal transduction.. Curr Opin Microbiol 2000 Apr;3(2):165-70.
    doi: 10.1016/s1369-5274(00)00070-9pubmed: 10745001google scholar: lookup
  42. Graham MR, Smoot LM, Migliaccio CA, Virtaneva K, Sturdevant DE, Porcella SF, Federle MJ, Adams GJ, Scott JR, Musser JM. Virulence control in group A Streptococcus by a two-component gene regulatory system: global expression profiling and in vivo infection modeling.. Proc Natl Acad Sci U S A 2002 Oct 15;99(21):13855-60.
    doi: 10.1073/pnas.202353699pmc: PMC129787pubmed: 12370433google scholar: lookup
  43. Martin B, Quentin Y, Fichant G, Claverys JP. Independent evolution of competence regulatory cascades in streptococci?. Trends Microbiol 2006 Aug;14(8):339-45.
    doi: 10.1016/j.tim.2006.06.007pubmed: 16820295google scholar: lookup
  44. Beres SB, Sesso R, Pinto SW, Hoe NP, Porcella SF, Deleo FR, Musser JM. Genome sequence of a Lancefield group C Streptococcus zooepidemicus strain causing epidemic nephritis: new information about an old disease.. PLoS One 2008 Aug 21;3(8):e3026.
    doi: 10.1371/journal.pone.0003026pmc: PMC2516327pubmed: 18716664google scholar: lookup
  45. Beaulaurier J, Schadt EE, Fang G. Deciphering bacterial epigenomes using modern sequencing technologies.. Nat Rev Genet 2019 Mar;20(3):157-172.
    doi: 10.1038/s41576-018-0081-3pmc: PMC6555402pubmed: 30546107google scholar: lookup
  46. Kobayashi I, Nobusato A, Kobayashi-Takahashi N, Uchiyama I. Shaping the genome--restriction-modification systems as mobile genetic elements.. Curr Opin Genet Dev 1999 Dec;9(6):649-56.
    doi: 10.1016/S0959-437X(99)00026-Xpubmed: 10607611google scholar: lookup
  47. Conlan S, Thomas PJ, Deming C, Park M, Lau AF, Dekker JP, Snitkin ES, Clark TA, Luong K, Song Y, Tsai YC, Boitano M, Dayal J, Brooks SY, Schmidt B, Young AC, Thomas JW, Bouffard GG, Blakesley RW, Mullikin JC, Korlach J, Henderson DK, Frank KM, Palmore TN, Segre JA. Single-molecule sequencing to track plasmid diversity of hospital-associated carbapenemase-producing Enterobacteriaceae.. Sci Transl Med 2014 Sep 17;6(254):254ra126.
    doi: 10.1126/scitranslmed.3009845pmc: PMC4203314pubmed: 25232178google scholar: lookup
  48. Sahu P, Pallaval Veera B. Quorum sensing in Streptococcus pyogenes and their role in establishment of disease. 2018 p 337–348.
    doi: 10.1007/978-981-13-2429-1_23google scholar: lookup
  49. Xie Z, Meng K, Yang X, Liu J, Yu J, Zheng C, Cao W, Liu H. Identification of a Quorum Sensing System Regulating Capsule Polysaccharide Production and Biofilm Formation in Streptococcus zooepidemicus.. Front Cell Infect Microbiol 2019;9:121.
    doi: 10.3389/fcimb.2019.00121pmc: PMC6482233pubmed: 31058104google scholar: lookup
  50. Balbontín R, Rowley G, Pucciarelli MG, López-Garrido J, Wormstone Y, Lucchini S, García-Del Portillo F, Hinton JC, Casadesús J. DNA adenine methylation regulates virulence gene expression in Salmonella enterica serovar Typhimurium.. J Bacteriol 2006 Dec;188(23):8160-8.
    doi: 10.1128/JB.00847-06pmc: PMC1698197pubmed: 16997949google scholar: lookup
  51. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH, Phillippy AM. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation.. Genome Res 2017 May;27(5):722-736.
    doi: 10.1101/gr.215087.116pmc: PMC5411767pubmed: 28298431google scholar: lookup
  52. Jolley KA, Bliss CM, Bennett JS, Bratcher HB, Brehony C, Colles FM, Wimalarathna H, Harrison OB, Sheppard SK, Cody AJ, Maiden MCJ. Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain.. Microbiology (Reading) 2012 Apr;158(Pt 4):1005-1015.
    doi: 10.1099/mic.0.055459-0pmc: PMC3492749pubmed: 22282518google scholar: lookup
  53. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, Olson R, Overbeek R, Parrello B, Pusch GD, Shukla M, Thomason JA 3rd, Stevens R, Vonstein V, Wattam AR, Xia F. RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes.. Sci Rep 2015 Feb 10;5:8365.
    doi: 10.1038/srep08365pmc: PMC4322359pubmed: 25666585google scholar: lookup
  54. Ozer EA. ClustAGE: a tool for clustering and distribution analysis of bacterial accessory genomic elements.. BMC Bioinformatics 2018 Apr 20;19(1):150.
    doi: 10.1186/s12859-018-2154-xpmc: PMC5910555pubmed: 29678129google scholar: lookup
  55. R Core Team. R: a language and environment for statistical computing. 2020.
  56. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks.. Genome Res 2003 Nov;13(11):2498-504.
    doi: 10.1101/gr.1239303pmc: PMC403769pubmed: 14597658google scholar: lookup
  57. Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, Fridman WH, Pagès F, Trajanoski Z, Galon J. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks.. Bioinformatics 2009 Apr 15;25(8):1091-3.
    doi: 10.1093/bioinformatics/btp101pmc: PMC2666812pubmed: 19237447google scholar: lookup
  58. Yu NY, Wagner JR, Laird MR, Melli G, Rey S, Lo R, Dao P, Sahinalp SC, Ester M, Foster LJ, Brinkman FS. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes.. Bioinformatics 2010 Jul 1;26(13):1608-15.
    doi: 10.1093/bioinformatics/btq249pmc: PMC2887053pubmed: 20472543google scholar: lookup
  59. Treangen TJ, Ondov BD, Koren S, Phillippy AM. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes.. Genome Biol 2014;15(11):524.
    doi: 10.1186/s13059-014-0524-xpmc: PMC4262987pubmed: 25410596google scholar: lookup
  60. Wickham H. ggplot2: elegant graphics for data analysis. 2016.
  61. Davis JJ, Wattam AR, Aziz RK, Brettin T, Butler R, Butler RM, Chlenski P, Conrad N, Dickerman A, Dietrich EM, Gabbard JL, Gerdes S, Guard A, Kenyon RW, Machi D, Mao C, Murphy-Olson D, Nguyen M, Nordberg EK, Olsen GJ, Olson RD, Overbeek JC, Overbeek R, Parrello B, Pusch GD, Shukla M, Thomas C, VanOeffelen M, Vonstein V, Warren AS, Xia F, Xie D, Yoo H, Stevens R. The PATRIC Bioinformatics Resource Center: expanding data and analysis capabilities.. Nucleic Acids Res 2020 Jan 8;48(D1):D606-D612.
    doi: 10.1093/nar/gkz943pmc: PMC7145515pubmed: 31667520google scholar: lookup
  62. Argimón S, Abudahab K, Goater RJE, Fedosejev A, Bhai J, Glasner C, Feil EJ, Holden MTG, Yeats CA, Grundmann H, Spratt BG, Aanensen DM. Microreact: visualizing and sharing data for genomic epidemiology and phylogeography.. Microb Genom 2016 Nov;2(11):e000093.
    pmc: PMC5320705pubmed: 28348833doi: 10.1099/mgen.0.000093google scholar: lookup
  63. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features.. Bioinformatics 2010 Mar 15;26(6):841-2.
    doi: 10.1093/bioinformatics/btq033pmc: PMC2832824pubmed: 20110278google scholar: lookup
  64. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction.. BMC Bioinformatics 2012 Jun 18;13:134.
    doi: 10.1186/1471-2105-13-134pmc: PMC3412702pubmed: 22708584google scholar: lookup

Citations

This article has been cited 2 times.
  1. Wan J, Weldon E, Ganser G, Morris ERA, Hughes EV, Bordin AI, Heine PA, Hust M, Cohen ND, Gill JJ, Liu M. Immunogenic Streptococcus equi cell surface proteins identified by ORFeome phage display. mSphere 2025 Dec 23;10(12):e0062625.
    doi: 10.1128/msphere.00626-25pubmed: 41288106google scholar: lookup
  2. Cito F, Di Francesco CE, Averaimo D, Chiaverini A, Alessiani A, Di Domenico M, Cresci M, Rulli M, Cantelmi MC, Di Bernardo MD, Giammarino A, Vincifori G, Petrini A. Streptococcus equi subsp. zooepidemicus: Epidemiological and Genomic Findings of an Emerging Pathogen in Central Italy. Animals (Basel) 2025 May 8;15(10).
    doi: 10.3390/ani15101351pubmed: 40427230google scholar: lookup
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