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Virulence factors, antimicrobial resistance and phylogeny of bovine mastitis-associated Streptococcus dysgalactiae

Published online by Cambridge University Press:  12 April 2023

Bruna Lourenço Crippa ,
Marjory Xavier Rodrigues ,
Tiago Tomazi ,
Yongqiang Yang ,
Liliana de Oliveira Rocha ,
Rodrigo Carvalho Bicalho  and
Nathália Cristina Cirone Silva
Bruna Lourenço Crippa*
Affiliation:
Department of Food Science and Nutrition, Faculty of Food Engineering (FEA), University of Campinas (UNICAMP), Campinas, SP 13083-862, Brazil
Marjory Xavier Rodrigues
Affiliation:
Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA
Tiago Tomazi
Affiliation:
Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA
Yongqiang Yang
Affiliation:
Department of Microbiology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, China
Liliana de Oliveira Rocha
Affiliation:
Department of Food Science and Nutrition, Faculty of Food Engineering (FEA), University of Campinas (UNICAMP), Campinas, SP 13083-862, Brazil
Rodrigo Carvalho Bicalho
Affiliation:
Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA
Nathália Cristina Cirone Silva
Affiliation:
Department of Food Science and Nutrition, Faculty of Food Engineering (FEA), University of Campinas (UNICAMP), Campinas, SP 13083-862, Brazil Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA
*
Author for correspondence: Bruna Lourenço Crippa, Email: lourencobruna@yahoo.com.br
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Abstract

We carried out a thorough genetic evaluation of Streptococcus dysgalactiae isolated from clinical bovine mastitis cases and performed a phylogenetic analysis to represent the evolutionary relationship between S. dysgalactiae sequences. A total of 35 S. dysgalactiae strains were isolated from cases of clinical mastitis identified at a large commercial dairy farm located near Ithaca, New York. Whole-genome sequencing identified twenty-six antibiotic resistance genes, four of which were acquired genes, in addition to fifty virulence genes. Multi-locus sequence typing detected three new sequence types (STs). We conclude that a high proportion of this microorganism carries multiple virulence determinants and resistance genes, and that this indicates its potential to cause mastitis. Eight different STs were identified, of which ST453 (n = 17) was the most prevalent and ST714, ST715, ST716 were novel STs.

Keywords

Genomic analysismastitis milkstreptococci
Type
Research Article
Information
Journal of Dairy Research , Volume 90 , Issue 2 , May 2023 , pp. 152 - 157
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press on behalf of Hannah Dairy Research Foundation

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References

Abd, H, Saed, EMR, Mohamed, H and Ibrahim, M (2020) Antimicrobial profile of multidrug-resistant Streptococcus spp isolated from dairy cows with clinical mastitis. Journal of Advanced Veterinary and Animal Research 7, 186–197.Google Scholar
Bettanin, J, Virmond, MP, Franciscato, C, Firmino, A and Neto, S (2019) Frequency of isolation of the bovine mastitis pathogens from southwest of Paran. Brazilian Journal of Hygiene and Animal Sanity 13, 440–451.Google Scholar
Calonzi, D, Romano, A, Monistero, V, Moroni, P, Luini, MV, Biscarini, F, Castiglioni, B and Cremonesi, P (2020) Technical note: development of multiplex PCR assays for the molecular characterization of Streptococcus uberis strains isolated from bovine mastitis. Journal of Dairy Science 103, 915–921.Google Scholar
Calvinho, LF, Almeida, RA and Oliver, SP (1998) Potential virulence factors of Streptococcus dysgalactiae associated with bovine mastitis. Veterinary Microbiology 61, 93–110.Google Scholar
Davis, CA and Janssen, EML (2020) Environmental fate processes of antimicrobial peptides daptomycin bacitracins and polymyxins. Environment International 134, 105–271.CrossRefGoogle ScholarPubMed
Gomes, F and Henriques, M (2016) Control of bovine mastitis: old and recent therapeutic approaches. Current Microbiology 72, 377–382.CrossRefGoogle ScholarPubMed
Grossman, TH (2016) Tetracycline antibiotics and resistance. Cold Spring Harbor Perspectives in Medicine 6, a025387.CrossRefGoogle ScholarPubMed
Haenni, M, Lupo, A and Madec, JY (2018) Antimicrobial resistance in Streptococcus spp. Microbiology Spectrum 6, doi: 10.1128/microbiolspec.ARBA-0008-2017.CrossRefGoogle ScholarPubMed
Hasegawa, T, Torii, K, Hashikawa, S, Iinuma, Y and Ohta, M (2002) Cloning and characterization of two novel DNases from Streptococcus pyogenes. Archives of Microbiology 177, 451–456.Google Scholar
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Meintjes, P and Drummond, A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.CrossRefGoogle ScholarPubMed
Latini, L, Ronchetti, MP, Merolla, R, Guglielmi, F, Bajaksouzian, S, Villa, MP, Jacobs, MR and Ronchetti, R (1999) Prevalence of mefE, erm and tet(M) genes in Streptococcus pneumoniae strains from central Italy. International Journal of Antimicrobial Agents 13, 29–33.Google Scholar
Matsue, M, Ogura, K, Sugiyama, H, Miyoshi-Akiyama, T, Takemori-Sakai, Y, Iwata, Y, Wada, T and Okamoto, S (2020) Pathogenicity characterization of prevalent-type Streptococcus dysgalactiae subsp equisimilis strains. Frontiers in Microbiology 11, 1–13.Google Scholar
Miller-Torbert, TA, Sharma, S and Holt, RG (2008) Inactivation of a gene for a fibronectin-binding protein of the oral bacterium Streptococcus mutans partially impairs its adherence to fibronectin. Microbial Pathogenesis 45, 53–59.CrossRefGoogle ScholarPubMed
Ota, Y, Furuhashi, K, Hayashi, W, Hirai, N and Ishikawa, J (2021) Daptomycin resistant Enterococcus faecalis has a mutation in liaX which encodes a surface protein that inhibits the LiaFSR systems and cell membrane remodeling. Journal of Infection and Chemotherapy 27, 90–93.CrossRefGoogle Scholar
Rato, MG, Nerlich, A, Bergmann, R, Bexiga, R and Nunes, SF, Vilela, CL, Santos-Sanches, I and Chhatwal, GS (2011) Virulence gene pool detected in bovine group C Streptococcus dysgalactiae subsp dysgalactiae isolates by use of a group A S pyogenes virulence microarray. Journal of Clinical Microbiology 49, 2470–2479.CrossRefGoogle Scholar
Saeed, SI, Mergani, A, Aklilu, E and Kamaruzzman, NF (2022) Antimicrobial peptides: bringing solution to the rising threats of antimicrobial resistance in livestock. Frontiers in Veterinary Science 9, 851052.Google Scholar
Samanta, I and Bandyopadhyay, S (2020) Resistance to aminoglycoside tetracycline and macrolides. In Samanta, I and Bandyopadhyay, S (eds), Antimicrobial Resistance in Agriculture. Amsterdam: Elsevier Science Direct, pp. 81–95.CrossRefGoogle Scholar
Sharma, P, Garg, N, Sharma, A, Capalash, N and Singh, R (2019) Nucleases of bacterial pathogens as virulence factors, therapeutic targets and diagnostic markers. International Journal of Medical Microbiology 309, 151–354.Google Scholar
Silva, NCC, Yang, Y, Rodrigues, MX, Tomazi, T and Bicalho, RC (2021) Whole-genome sequencing reveals high genetic diversity of Streptococcus uberis isolated from cows with mastitis. BMC Veterinary Research 17, 1–15.CrossRefGoogle ScholarPubMed
Smeesters, PR, Drèze, PA, Perez-Morga, D, Biarent, D, Van Melderen, L and Vergison, A (2010) Group A Streptococcus virulence and host factors in two toddlers with rheumatic fever following toxic shock syndrome. International Journal of Infectious Diseases 14, 403–409.CrossRefGoogle ScholarPubMed
Taylor, SD and Palmer, M (2016) The action mechanism of daptomycin. Bioorganic and Medicinal Chemistry 24, 6253–6268.CrossRefGoogle ScholarPubMed
Tian, XY, Zheng, N, Han, RW, Ho, H, Wang, J, Wang, YT, Wang, SQ, Li, HG, Liu, HW and Yu, ZN (2019) Antimicrobial resistance and virulence genes of Streptococcus isolated from dairy cows with mastitis in China. Microbial Pathogenesis 131, 33–39.Google Scholar
Tomazi, T, Sumnicht, M, Tomazi, ACCH, Silva, JCC, Bringhenti, L, Duarte, LM, Silva, MMM, Rodrigues, MX and Bicalho, RC (2021) Negatively controlled randomized clinical trial comparing different antimicrobial interventions for treatment of clinical mastitis caused by Gram-positive pathogens. Journal of Dairy Science 104, 3364–3385.CrossRefGoogle ScholarPubMed
Tomlinson, JH, Kalverda, AP and Calabrese, AN (2020) Fusidic acid resistance through changes in the dynamics of the drug target. Proceedings of the National Academy of Sciences of the United States of America 117, 2523–2553.Google ScholarPubMed
Ulsenheimer, BC, Amarante, GM, Rosa, SKD, Ziegler, SJ, Piccinini, CN, Beck, C, Viero, LM and Martins, LRV (2020) Perfil de sensibilidade e casuística do Streptococcus dysgalactiae em mastites na região Noroeste do Estado do RS. Pubvet 14, 1–6.Google Scholar
Vélez, JR, Cameron, M, Rodríguez-Lecompte, JC, Xia, F, Heider, LC, Saab, M, Trenton McClure, J and Sánchez, J (2017) Whole-genome sequence analysis of antimicrobial resistance genes in Streptococcus uberis and Streptococcus dysgalactiae isolates from Canadian dairy herds. Frontiers in Veterinary Science 4, 1–11.CrossRefGoogle ScholarPubMed
Wang, QB, Xu, Y, Gu, Z, Liu, N, Jin, K, Li, Y, Crabbe, MJC and Zhong, Y (2018) Identification of new antibacterial targets in RNA polymerase of Mycobacterium tuberculosis by detecting positive selection sites. Computational Biology and Chemistry 73, 25–30.CrossRefGoogle ScholarPubMed
Wilson, DN (2020) Target protection as a key antibiotic resistance mechanism. Nature Reviews Microbiology 18, 637–648.CrossRefGoogle ScholarPubMed
Zhang, S, Piepers, S, Shan, R, Cai, L, Mao, S, Zou, J, Ali, T, De Vlieghe, S and Han, B (2018) Phenotypic and genotypic characterization of antimicrobial resistance profiles in Streptococcus dysgalactiae isolated from bovine clinical mastitis in 5 provinces of China. Journal of Dairy Science 101, 3344–3355.Google Scholar
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