Genetic characterization of Streptococcus equi subspecies zooepidemicus associated with high swine mortality in the United States.
bacterial pathogens
emerging diseases
veterinary epidemiology
Journal
Transboundary and emerging diseases
ISSN: 1865-1682
Titre abrégé: Transbound Emerg Dis
Pays: Germany
ID NLM: 101319538
Informations de publication
Date de publication:
Nov 2020
Nov 2020
Historique:
received:
24
03
2020
revised:
21
04
2020
accepted:
15
05
2020
pubmed:
28
5
2020
medline:
9
1
2021
entrez:
28
5
2020
Statut:
ppublish
Résumé
High mortality events due to Streptococcus equi subspecies zooepidemicus (Streptococcus zooepidemicus) in swine have not previously been reported in the United States. In September and October 2019, outbreaks with swine mortality up to 50% due to S. zooepidemicus septicaemia were reported in Ohio and Tennessee. Genomic epidemiological analysis revealed that the eight outbreak isolates were clustered together with ATCC 35246, a Chinese strain caused outbreaks with high mortality, also closely related to three isolates from human cases from Virginia, but significantly different from an outbreak-unrelated swine isolate from Arizona and most isolates from other animal species. Comparative genomic analysis on two outbreak isolates and another outbreak-unrelated isolate identified several genomic islands and virulence genes specifically in the outbreak isolates only, which are likely associated with the high mortality observed in the swine population. These findings have implications for understanding, tracking and possibly preventing diseases caused by S. zooepidemicus in swine.
Substances chimiques
DNA, Bacterial
0
Banques de données
GENBANK
['CP002904.1', 'CP006770.1', 'CP046040', 'CP046042', 'CP046041']
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2797-2808Subventions
Organisme : Swine Health Information Center
ID : SHIC#19-236
Informations de copyright
© 2020 Blackwell Verlag GmbH.
Références
Abbott, Y., Acke, E., Khan, S., Muldoon, E. G., Markey, B. K., Pinilla, M., … Waller, A. (2010). Zoonotic transmission of Streptococcus equi subsp. zooepidemicus from a dog to a handler. Journal of Medical Microbiology, 59(Pt 1), 120-123. https://doi.org/10.1099/jmm.0.012930-0
Alber, J., El-Sayed, A., Estoepangestie, S., Lammler, C., & Zschock, M. (2005). Dissemination of the superantigen encoding genes seeL, seeM, szeL and szeM in Streptococcus equi subsp. equi and Streptococcus equi subsp. zooepidemicus. Veterinary Microbiology, 109(1-2), 135-141. https://doi.org/10.1016/j.vetmic.2005.05.001
Alikhan, N. F., Petty, N. K., Ben Zakour, N. L., & Beatson, S. A. (2011). BLAST Ring Image Generator (BRIG): Simple prokaryote genome comparisons. BMC Genomics, 12, 402. https://doi.org/10.1186/1471-2164-12-402
Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., … Pevzner, P. A. (2012). SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology, 19(5), 455-477. https://doi.org/10.1089/cmb.2012.0021
Beres, S. B., Sesso, R., Pinto, S. W., Hoe, N. P., Porcella, S. F., Deleo, F. R., & Musser, J. M. (2008). Genome sequence of a Lancefield group C Streptococcus zooepidemicus strain causing epidemic nephritis: New information about an old disease. PLoS ONE, 3(8), e3026. https://doi.org/10.1371/journal.pone.0003026
Bergmann, R., Jentsch, M. C., Uhlig, A., Muller, U., van der Linden, M., Rasmussen, M., … Baums, C. G. (2019). Prominent binding of human and equine fibrinogen to Streptococcus equi subsp. zooepidemicus is mediated by specific SzM-types and is a distinct phenotype of zoonotic isolates. Infection and Immunity, 88(1), e00559-19. https://doi.org/10.1128/IAI.00559-19
Bertelli, Claire, Laird, Matthew R., Williams, Kelly P., Lau, Britney Y., Hoad, Gemma, Winsor, Geoffrey L., & Brinkman, Fiona S. L. (2017). IslandViewer 4: expanded prediction of genomic islands for larger-scale datasets. Nucleic Acids Research, 45(W1), W30-W35. https://doi.org/10.1093/nar/gkx343
Blum, S., Elad, D., Zukin, N., Lysnyansky, I., Weisblith, L., Perl, S., … David, D. (2010). Outbreak of Streptococcus equi subsp. zooepidemicus infections in cats. Veterinary Microbiology, 144(1-2), 236-239. https://doi.org/10.1016/j.vetmic.2009.12.040
Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30(15), 2114-2120. https://doi.org/10.1093/bioinformatics/btu170
Bordes-Benítez, A., Sánchez-Oñoro, M., Suárez-Bordón, P., García-Rojas, A. J., Saéz-Nieto, J. A., González-García, A., … Bolaños-Rivero, M. (2006). Outbreak of Streptococcus equi subsp. zooepidemicus infections on the island of Gran Canaria associated with the consumption of inadequately pasteurized cheese. European Journal of Clinical Microbiology and Infectious Diseases, 25(4), 242-246. https://doi.org/10.1007/s10096-006-0119-x
Byun, J. W., Yoon, S. S., Woo, G. H., Jung, B. Y., & Joo, Y. S. (2009). An outbreak of fatal hemorrhagic pneumonia caused by Streptococcus equi subsp. zooepidemicus in shelter dogs. Journal of Veterinary Science, 10(3), 269-271. https://doi.org/10.4142/jvs.2009.10.3.269
Fan, H., Wang, Y., Tang, F., & Lu, C. (2008). Determination of the mimic epitope of the M-like protein adhesin in swine Streptococcus equi subsp. zooepidemicus. BMC Microbiology, 8, 170. https://doi.org/10.1186/1471-2180-8-170
Fraser, J., Arcus, V., Kong, P., Baker, E., & Proft, T. (2000). Superantigens - powerful modifiers of the immune system. Mol Med Today, 6(3), 125-132. https://doi.org/10.1016/s1357-4310(99)01657-3
Fulde, M., & Valentin-Weigand, P. (2013). Epidemiology and pathogenicity of zoonotic streptococci. Current Topics in Microbiology and Immunology, 368, 49-81. https://doi.org/10.1007/82_2012_277
Gardner, S. N., Slezak, T., & Hall, B. G. (2015). kSNP3. 0: SNP detection and phylogenetic analysis of genomes without genome alignment or reference genome. Bioinformatics, 31(17), 2877-2878. https://doi.org/10.1093/bioinformatics/btv271
Gruszynski, K., Young, A., Levine, S. J., Garvin, J. P., Brown, S., Turner, L., … Beall, B. (2015). Streptococcus equi subsp. zooepidemicus infections associated with guinea pigs. Emerging Infectious Diseases, 21(1), 156-158. https://doi.org/10.3201/eid2101.140640
Jolley, K. A., Chan, M. S., & Maiden, M. C. (2004). mlstdbNet - distributed multi-locus sequence typing (MLST) databases. BMC Bioinformatics, 5, 86. https://doi.org/10.1186/1471-2105-5-86
Kelly, C., Bugg, M., Robinson, C., Mitchell, Z., Davis-Poynter, N., Newton, J. R., … Waller, A. S. (2006). Sequence variation of the SeM gene of Streptococcus equi allows discrimination of the source of strangles outbreaks. Journal of Clinical Microbiology, 44(2), 480-486. https://doi.org/10.1128/JCM.44.2.480-486.2006
Kittang, B. R., Pettersen, V. K., Oppegaard, O., Skutlaberg, D. H., Dale, H., Wiker, H. G., & Skrede, S. (2017). Zoonotic necrotizing myositis caused by Streptococcus equi subsp. zooepidemicus in a farmer. BMC Infectious Diseases, 17(1), 147. https://doi.org/10.1186/s12879-017-2262-7
Kuusi, M., Lahti, E., Virolainen, A., Hatakka, M., Vuento, R., Rantala, L., … Huotari, K. (2006). An outbreak of Streptococcus equi subspecies zooepidemicus associated with consumption of fresh goat cheese. BMC Infectious Diseases, 6, 36. https://doi.org/10.1186/1471-2334-6-36
Laus, F., Preziuso, S., Spaterna, A., Beribe, F., Tesei, B., & Cuteri, V. (2007). Clinical and epidemiological investigation of chronic upper respiratory diseases caused by beta-haemolytic Streptococci in horses. Comparative Immunology, Microbiology and Infectious Diseases, 30(4), 247-260. https://doi.org/10.1016/j.cimid.2007.02.003
Letunic, I., & Bork, P. (2019). Interactive Tree Of Life (iTOL) v4: Recent updates and new developments. Nucleic Acids Research, 47(W1), W256-W259. https://doi.org/10.1093/nar/gkz239
Ma, Z., Geng, J., Yi, L. I., Xu, B., Jia, R., Li, Y., … Hu, S. (2013). Insight into the specific virulence related genes and toxin-antitoxin virulent pathogenicity islands in swine streptococcosis pathogen Streptococcus equi ssp. zooepidemicus strain ATCC35246. BMC Genomics, 14, 377. https://doi.org/10.1186/1471-2164-14-377
Ma, Z., Geng, J., Zhang, H., Yu, H., Yi, L., Lei, M., … Hu, S. (2011). Complete genome sequence of Streptococcus equi subsp. zooepidemicus strain ATCC 35246. Journal of Bacteriology, 193(19), 5583-5584. https://doi.org/10.1128/JB.05700-11
Ma, Z., Peng, J., Yu, D., Park, J. S., Lin, H., Xu, B., … Waldor, M. K. (2019). A streptococcal Fic domain-containing protein disrupts blood-brain barrier integrity by activating moesin in endothelial cells. PLoS Pathogens, 15(5), e1007737. https://doi.org/10.1371/journal.ppat.1007737
Ma, Z., Zhang, H., Zheng, J., Li, Y., Yi, L., Fan, H., & Lu, C. (2012). Interaction between M-like protein and macrophage thioredoxin facilitates antiphagocytosis for Streptococcus equi ssp. zooepidemicus. PLoS ONE, 7(2), e32099. https://doi.org/10.1371/journal.pone.0032099
Metzgar, D., & Zampolli, A. (2011). The M protein of group A Streptococcus is a key virulence factor and a clinically relevant strain identification marker. Virulence, 2(5), 402-412. https://doi.org/10.4161/viru.2.5.16342
Mikheenko, A., Prjibelski, A., Saveliev, V., Antipov, D., & Gurevich, A. (2018). Versatile genome assembly evaluation with QUAST-LG. Bioinformatics, 34(13), i142-i150. https://doi.org/10.1093/bioinformatics/bty266
Minces, L. R., Brown, P. J., & Veldkamp, P. J. (2011). Human meningitis from Streptococcus equi subsp. zooepidemicus acquired as zoonoses. Epidemiology and Infection, 139(3), 406-410. https://doi.org/10.1017/S0950268810001184
Newton, J. R., Laxton, R., Wood, J. L., & Chanter, N. (2008). Molecular epidemiology of Streptococcus zooepidemicus infection in naturally occurring equine respiratory disease. The Veterinary Journal, 175(3), 338-345. https://doi.org/10.1016/j.tvjl.2007.02.018
Paillot, R., Darby, A. C., Robinson, C., Wright, N. L., Steward, K. F., Anderson, E., … Waller, A. S. (2010). Identification of three novel superantigen-encoding genes in Streptococcus equi subsp. zooepidemicus, szeF, szeN, and szeP. Infection and Immunity, 78(11), 4817-4827. https://doi.org/10.1128/IAI.00751-10
Paillot, R., Robinson, C., Steward, K., Wright, N., Jourdan, T., Butcher, N., … Waller, A. S. (2010). Contribution of each of four Superantigens to Streptococcus equi-induced mitogenicity, gamma interferon synthesis, and immunity. Infection and Immunity, 78(4), 1728-1739. https://doi.org/10.1128/IAI.01079-09
Pelkonen, S., Lindahl, S. B., Suomala, P., Karhukorpi, J., Vuorinen, S., Koivula, I., … Tuuminen, T. (2013). Transmission of Streptococcus equi subspecies zooepidemicus infection from horses to humans. Emerging Infectious Diseases, 19(7), 1041-1048. https://doi.org/10.3201/eid1907.121365
Pesavento, P. A., Hurley, K. F., Bannasch, M. J., Artiushin, S., & Timoney, J. F. (2008). A clonal outbreak of acute fatal hemorrhagic pneumonia in intensively housed (shelter) dogs caused by Streptococcus equi subsp. zooepidemicus. Veterinary Pathology, 45(1), 51-53. https://doi.org/10.1354/vp.45-1-51
Priestnall, S., & Erles, K. (2011). Streptococcus zooepidemicus: An emerging canine pathogen. The Veterinary Journal, 188(2), 142-148. https://doi.org/10.1016/j.tvjl.2010.04.028
Rash, N. L., Robinson, C., DeSouza, N., Nair, S., Hodgson, H., Steward, K., … Paillot, R. (2014). Prevalence and disease associations of superantigens szeF, szeN and szeP in the S. zooepidemicus population and possible functional redundancy of szeF. Research in Veterinary Science, 97(3), 481-487. https://doi.org/10.1016/j.rvsc.2014.09.001
Sesso, R., & Pinto, S. W. (2005). Five-year follow-up of patients with epidemic glomerulonephritis due to Streptococcus zooepidemicus. Nephrology, Dialysis, Transplantation, 20(9), 1808-1812. https://doi.org/10.1093/ndt/gfh904
Sharp, M. W., Prince, M. J., & Gibbens, J. (1995). S zooepidemicus infection and bovine mastitis. The Veterinary Record, 137(5), 128. https://doi.org/10.1136/vr.137.5.128-b
Soedarmanto, I., Pasaribu, F. H., Wibawan, I. W., & Lammler, C. (1996). Identification and molecular characterization of serological group C streptococci isolated from diseased pigs and monkeys in Indonesia. Journal of Clinical Microbiology, 34(9), 2201-2204. https://doi.org/10.1128/JCM.34.9.2201-2204.1996
Tatusova, T., DiCuccio, M., Badretdin, A., Chetvernin, V., Nawrocki, E. P., Zaslavsky, L., … Ostell, J. (2016). NCBI prokaryotic genome annotation pipeline. Nucleic Acids Research, 44(14), 6614-6624. https://doi.org/10.1093/nar/gkw569
Timoney, J. F. (2004). The pathogenic equine streptococci. Veterinary Research, 35(4), 397-409. https://doi.org/10.1051/vetres:2004025
Torres, R., Santos, T. Z., Bernardes, A. F. L., Soares, P. A., Soares, A. C. C., & Dias, R. S. (2018). Outbreak of Glomerulonephritis Caused by Streptococcus zooepidemicus SzPHV5 Type in Monte Santo de Minas, Minas Gerais, Brazil. Journal of Clinical Microbiology, 56(10), e00845-18. https://doi.org/10.1128/JCM.00845-18
Velineni, S., & Timoney, J. F. (2013). Characterization and protective immunogenicity of the SzM protein of Streptococcus zooepidemicus NC78 from a clonal outbreak of equine respiratory disease. Clinical and Vaccine Immunology, 20(8), 1181-1188. https://doi.org/10.1128/CVI.00069-13
Walker, J. A., & Timoney, J. F. (1998). Molecular basis of variation in protective SzP proteins of Streptococcus zooepidemicus. American Journal of Veterinary Research, 59(9), 1129-1133.
Webb, K., Jolley, K. A., Mitchell, Z., Robinson, C., Newton, J. R., Maiden, M. C. J., & Waller, A. (2008). Development of an unambiguous and discriminatory multilocus sequence typing scheme for the Streptococcus zooepidemicus group. Microbiology, 154(Pt 10), 3016-3024. https://doi.org/10.1099/mic.0.2008/018911-0
Wick, R. R., Judd, L. M., Gorrie, C. L., & Holt, K. E. (2017). Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Computational Biology, 13(6), e1005595. https://doi.org/10.1371/journal.pcbi.1005595
Xu, B., Zhang, P., Zhou, H., Sun, Y., Tang, J., & Fan, H. (2019). Identification of novel genes associated with anti-phagocytic functions in Streptococcus equi subsp. zooepidemicus. Veterinary Microbiology, 233, 28-38. https://doi.org/10.1016/j.vetmic.2019.04.023