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Biofilm forming multidrug resistant Staphylococcus aureus of dairy origin: molecular and evolutionary perspectives | ||
| Iranian Journal of Veterinary Research | ||
| دوره 24، شماره 3 - شماره پیاپی 84، 2023، صفحه 193-204 اصل مقاله (582.78 K) | ||
| نوع مقاله: Full paper (Original article) | ||
| شناسه دیجیتال (DOI): 10.22099/ijvr.2023.43941.6445 | ||
| نویسندگان | ||
| A. Ahmed1؛ M. Ijaz* 2؛ J. A. Khan3؛ A. A. Anjum4 | ||
| 1Ph.D. Student in Veterinary Medicine, Department of Veterinary Medicine, University of Veterinary and Animal Sciences, Lahore, Pakistan | ||
| 2Department of Veterinary Medicine, University of Veterinary and Animal Sciences, Lahore, Pakistan; 3Institute of Microbiology, University of Veterinary and Animal Sciences, Lahore, Pakistan | ||
| 3Department of Veterinary Medicine, University of Veterinary and Animal Sciences, Lahore, Pakistan | ||
| 4Institute of Microbiology, University of Veterinary and Animal Sciences, Lahore, Pakistan | ||
| چکیده | ||
| Background: Biofilm production by Staphylococcus aureus is a prevailing cause of multidrug resistance. The evolutionary mechanisms of adaption with host and pathogenicity are poorly understood. Aims: The present study aimed to investigate the biofilm-forming potential, associated multidrug resistance, and the evolutionary analysis of S. aureus isolated from bovine subclinical mastitis. Methods: 122 S. aureus isolates were subjected to Congo red agar method (CRA), microtitre plate method (MTP), and PCR to check the biofilm-forming potential. The Kirby-Bauer disk diffusion method was used to evaluate the antibiotic resistance pattern. The icaA gene of isolates was subjected to molecular and evolutionary analysis using different bioinformatics tools. Results: The results showed that 63.93% of S. aureus isolates carried the icaA gene and the detection rate of CRA was higher (36.07%) compared to the MTP test (24.59%). A total of 78.21% and 56.41% of biofilm-positive isolates were methicillin-resistant S. aureus (MRSA) and vancomycin-resistant S. aureus (VRSA), respectively. All S. aureus isolates (100%) showed multidrug resistance. The molecular analysis showed an evolutionary link between isolates and revealed a strong codon bias, three different recombination events, and positive selection in some residues of the semi-conserved segments of the icaA gene. Conclusion: The study concluded that biofilm-positive isolates have a high tendency to exhibit methicillin, vancomycin, and multidrug resistance. The findings suggest that mutation and selection are the most likely causes of codon bias in the icaA gene sequences. The variations led by recombination events and positive selection are suggestive of bacterial strategy to combat antimicrobial effects and to escape the host’s immune surveillance. | ||
| کلیدواژهها | ||
| Antimicrobial resistance؛ Biofilm؛ Evolutionary analysis؛ Mastitis؛ MRSA | ||
| مراجع | ||
|
Abdolahi, A and Khodavandi, A (2019). Antibacterial effects of vancomycin in combination with methicillin against methicillin-resistant and methicillinsensitive Staphylo-coccus aureus. J. Shahrekord Univ. Med. Sci., 21: 57-63. https://doi.org/10.34172/jsums.2019.10.
Abboud, Z; Galuppo, L; Tolone, M; Vitale, M; Puleio, R; Osman, M; Loria, GR and Hamze, M (2021). Molecular characterization of antimicrobial resistance and virulence genes of bacterial pathogens from bovine and caprine mastitis in northern Lebanon. Microorganisms. 9: 1-12. https://doi.org/10.3390/microorganisms9061148.
Abdul, M; Malik, R; Ijaz, M; Islam, A; Shahid, A; Farooqi, H and Hussain, K (2017). The prevalence and associated risk factors of Coa gene (Coagulase positive Staphylococcus aureus) from Bovine Milk Kafkas. Univ. Vet. Fak. Derg., 23: 809-815. doi: 10.9775/kvfd.2017. 17910.
Ahmed, A; Ijaz, M; Khan, JA and Anjum, AA (2022). Molecular characterization and therapeutic insights into biofilm positive Staphylococcus aureus isolated from bovine subclinical mastitis. Pak. Vet. J., 42: 584-590. https://doi.org/10.1186/s12917-015-0319-7.
Altaf, M; Ijaz, M; Ghaffar, A; Rehman, A and Avais, M (2019). Antibiotic susceptibility profile and synergistic effect of non-steroidal anti-inflammatory drugs on antibacterial activity of resistant antibiotics (Oxytetracycline and Gentamicin) against methicillin resistant Staphylococcus aureus (MRSA). Microb. Pathog., 137: 1-6. https://doi.org/10.1016/j.micpath.2019.103755.
Ansari, S; Nepal, HP; Gautam, R; Rayamajhi, N; Shrestha, S; Upadhyay, G; Acharya, A and Chapagain, ML (2014). Threat of drug resistant Staphylococcus aureus to health in Nepal. BMC Infect. Dis., 14: 1-5. https://doi.org/ 10.1186/1471-2334-14-157.
Aqib, AI; Ijaz, M; Farooqi, SH; Ahmed, R; Shoaib, M; Ali, MM; Mehmood, K and Zhang, H (2018). Emerging discrepancies in conventional and molecular epidemiology of methicillin resistant Staphylococcus aureus isolated from bovine milk. Microb. Pathog., 116: 38-43. https://doi.org/ 10.1016/j.micpath.2018.01.005.
Aslantaş, Ö and Demir, C (2016). Investigation of the antibiotic resistance and biofilm-forming ability of Staphylococcus aureus from subclinical bovine mastitis cases. J. Dairy Sci., 99: 8607-8613. https://doi.org/10.3168/ jds.2016-11310.
Ba, X; Harrison, EM; Edwards, GF; Holden, MT; Larsen, AR; Petersen, A; Skov, RL; Peacock, SJ; Parkhill, J; Paterson, GK and Holmes, MA (2014). Novel mutations in penicillin-binding protein genes in clinical Staphylococcus aureus isolates that are methicillin resistant on susceptibility testing, but lack the mec gene. J. Antimicrob. Chemother., 69: 594-597.
Begum, HA; Uddin, MS; Islam, MJ; Nazir, IM and Rahman, MT (2007). Detection of biofilm producing coagulase positive Staphylococcus aureus from bovine mastitis, their pigment production, hemolytic activity and antibiotic sensitivity pattern. Islam Z. Für Gesch. Kult. Islam Orients., 4: 97-100.
Chaudhry, V and Patil, PB (2020). Evolutionary insights into adaptation of Staphylococcus haemolyticus to human and non-human niches. Genomics. 112: 2052-2062.
Chen, L; Tang, ZY; Cui, SY; Ma, ZB; Deng, H; Kong, WL; Yang, LW; Lin, C; Xiong, WG and Zeng, ZL (2020). Biofilm production ability, virulence and antimicrobial resistance genes in Staphylococcus aureus from various veterinary hospitals. Pathogens. 9: 1-17. https://doi.org/ 10.3390/pathogens9040264.
CLSI (2019). Performance Standards for Antimicrobial Susceptibility Testing. 29th Edn.
DaSilva, B; DaMotta, CC; Barbieri, NL; de Melo, DA; Gomez, MA; de Alencar, TA; da Silva Coelho, I; de Oliveira Coelho, SD; Logue, CM and de Souza, MM (2021). Molecular characterization and genetic diversity of Staphylococcus aureus isolates of dairy production farms in Rio de Janeiro, Brazil. Rev. Bras. Med. Vet., 43: 1-12. https://doi.org/10.29374/2527-2179.BJVM001120.
Darwish, SF and Asfour, HAE (2013). Investigation of biofilm forming ability in staphylococci causing bovine mastitis using phenotypic and genotypic assays. Sci. World J., 2013: 1-9. https://doi.org/10.1155/2013/378492.
Driebe, EM; Sahl, JW; Roe, C; Bowers, JR; Schupp, JM; Gillece, JD; Kelley, E; Price, LB; Pearson, TR; Hepp, CM and Brzoska, PM (2015). Using whole genome analysis to examine recombination across diverse sequence types of Staphylococcus aureus. PLoS One. 10: e0130955. https://doi.org/10.1371/journal.pone.0130955.
Fabres-Klein, MH; Caizer, MJ; Contelli Klein, R; Nunes de Souza, G and de Oliveira Barros Ribon, A (2015). An association between milk and slime increases biofilm production by bovine Staphylococcus aureus. BMC Vet. Res. 11: 1-8. https://doi.org/10.1186/s12917-015-0319-7.
Fèvre, EM; Bronsvoort, BMDC; Hamilton, KA and Cleaveland, S (2006). Animal movements and the spread of infectious diseases. Trends Microbiol., 14: 125-131. https://doi.org/10.1016/j.tim.2006.01.004.
Ghumman, NZ; Ijaz, M; Ahmed, A; Javed, MU; Muzammil, I and Raza, A (2022). Evaluation of methicillin resistance in field isolates of Staphylococcus aureus: an emerging issue of indigenous bovine breeds. Pak. J. Zool., 2022: 1-12 https://dx.doi.org/10.17582/ journal.pjz/20220316080346.
Haddad, H; Schmelcher, M; Sabzalipoor, H; Seyed Hosseini, E and Moniri, R (2018). Recombinant endolysins as potential therapeutics against antibiotic-resistant Staphylococcus aureus: Current status of research and novel delivery strategies. Clin. Microbiol. Rev., 31: 1-17. https://doi.org/10.1128/CMR.00071-17.
Haran, KP; Godden, S; Boxrud, D; Jawahir, S; Bender, JB and Sreevatsan, S (2012). Prevalence and characterization of Staphylococcus aureus, including methicillin-resistant Staphylococcus aureus, isolated from bulk tank milk from Minnesota dairy farms. J. Clin. Microbiol., 50: 688-695. https://doi.org/10.1128/JCM.05214-11.
Hassan, A; Usman, J; Kaleem, F; Omair, M; Khalid, A and Iqbal, M (2011). Evaluation of different detection methods of biofilm formation in the clinical isolates. Brazilian J. Infect. Dis., 15: 305-311. https://doi.org/10.1590/S1413-86702011000400002.
He, JZ; Wang, AQ; Liu, G; Gao, J; Ali, T and Han, B (2014). Biofilm formation and biofilm-associated genes assay of Staphylococcus aureus isolated from bovine subclinical mastitis in China. Pak. Vet. J., 34: 508-513.
Hogan, JS; Gonzalez, RN; Harmon, RJ; Nickerson, SC; Oliver, SP; Pankey, JW and Smith, KL (1999). Laboratory handbook on bovine mastitis. Madison, WI, USA, NMC Inc.,
Hu, DL; Li, S; Fang, R and Ono, HK (2021). Update on molecular diversity and multipathogenicity of staphylococcal superantigen toxins. Anim. Dis., 1: 1-15. https://doi.org/10.1186/s44149-021-00007-7.
Islam, MA; Parveen, S; Rahman, M; Huq, M; Nabi, A; Khan, ZU; Ahmed, N and Wagenaar, JA (2019). Occurrence and characterization of methicillin resistant Staphylococcus aureus in processed raw foods and ready-to-eat foods in an urban setting of a developing country. Front. Microbiol., 10: 1-7. https://doi.org/10.3389/fmicb. 2019.00503.
Jain, A and Agarwal, A (2009). Biofilm production, a marker of pathogenic potential of colonizing and commensal staphylococci. J. Microbiol. Methods. 76: 88-92. https://doi.org/10.1016/j.mimet.2008.09.017.
Javed, MU; Ijaz, M; Durrani, AZ and Ali, MM (2023). On-farm epidemiology, virulence profiling, and molecular characterization of methicillin-resistant Staphylococcus aureus at goat farms. Microb. Pathogen., 185: 106456.
Javed, MU; Ijaz, M; Fatima, Z; Anjum, AA; Aqib, AI; Ali, MM; Rehman, A; Ahmed, A and Ghaffar, A (2021). Frequency and antimicrobial susceptibility of methicillin and vancomycin-resistant Staphylococcus aureus from bovine milk. Pak. Vet. J., 41: 463-468. http://dx.doi.org/10. 29261/pakvetj/2021.060.
Khoramrooz, SS; Mansouri, F; Marashifard, M; Hosseini, SA; Chenarestane-Olia, FA; Ganavehei, B; Gharibpour, F; Shahbazi, A; Mirzaii, M and Darban-Sarokhalil, D (2016). Detection of biofilm related genes, classical enterotoxin genes and agr typing among Staphylococcus aureus isolated from bovine with subclinical mastitis in southwest of Iran. Microb. Pathog., 97: 45-51. https://doi.org/10.1016/j.micpath.2016.05.022.
Koonin, EV and Wolf, YI (2010). Constraints and plasticity in genome and molecular-phenome evolution. Nat. Rev. Genet., 11: 487-498.
Koreen, L; Ramaswamy, SV; Graviss, EA; Naidich, S; Musser, JM and Kreiswirth, BN (2004). spa typing method for discriminating among Staphylococcus aureus isolates: implications for use of a single marker to detect genetic micro-and macrovariation. J. Clin. Microbiol., 42: 792-799. https://doi.org/10.1128%2FJCM.42.2.792-799. 2004.
Kouidhi, B; Zmantar, T; Hentati, H and Bakhrouf, A (2010). Cell surface hydrophobicity, biofilm formation, adhesives properties and molecular detection of adhesins genes in Staphylococcus aureus associated to dental caries. Microb. Pathog., 49: 14-22. https://doi.org/10.1016/j. micpath.2010.03.007.
Librado, P and Rozas, J (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 25: 1451-1452.
Louie, L; Matsumura, SO; Choi, E; Louie, M and Simor, AE (2000). Evaluation of three rapid methods for detection of methicillin resistance in Staphylococcus aureus. J. Clin. Microbiol., 38: 2170-2173. https://doi.org/10.1128/.38.6. 2170-2173.2000.
Malik, MA; Muhammad, IJ; Aqib, AI; Farooqi, SH and Hussain, K (2017). The prevalence and associated risk factors of coa gene (coagulase positive Staphylococcus aureus) from bovine milk. Kafkas Univ. Vet. Fak. Derg., 23: 809-815. https://doi.org/10.9775/kvfd.2017.17910.
Marques, VF; Motta, CC; Soares, BD; Melo, DA; Coelho, SD; Coelho, ID; Barbosa, HS and Souza, MM (2017). Biofilm production and beta-lactamic resistance in Brazilian Staphylococcus aureus isolates from bovine mastitis. Brazilian J. Microbiol., 48: 118-124. https://doi. org/10.1016/j.bjm.2016.10.001.
Melchior, MB; Vaarkamp, H and Fink-Gremmels, J (2006). Biofilms: A role in recurrent mastitis infections? Vet. J., 171: 398-407. https://doi.org/10.1016/j.tvjl.2005.01.006.
Melchior, MB; Van Osch, MHJ; Graat, RM; Van Duijkeren, E; Mevius, DJ; Nielen, M; Gaastra, W and Fink-Gremmels, J (2009). Biofilm formation and genotyping of Staphylococcus aureus bovine mastitis isolates: Evidence for lack of penicillin-resistance in Agr-type II strains. Vet. Microbiol., 137: 83-89. https://doi.org/ 10.1016/j.vetmic.2008.12.004.
Melo, PD; Ferreira, LM; Nader Filho, A; Zafalon, LF; Vicente, HI and Souza, VD (2013). Comparison of methods for the detection of biofilm formation by Staphylococcus aureus isolated from bovine subclinical mastitis. Brazilian J. Microbiol., 44: 119-124. https://doi. org/10.1590/S1517-83822013005000031.
Miragaia, M (2018). Factors contributing to the evolution of Meca-mediated β-lactam resistance in staphylococci: Update and new insights from whole genome sequencing (WGS). Front. Microbiol., 9: 1-16. https://doi.org/10.3389/ fmicb.2018.02723.
Nei, M and Gojobori, T (1986). Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol., 3: 418-426. https://doi.org/10.1093/OXFORDJOURNALS. MOLBEV.A040410.
Neopane, P; Nepal, HP; Shrestha, R; Uehara, O and Abiko, Y (2018). In vitro biofilm formation by Staphylococcus aureus isolated from wounds of hospital-admitted patients and their association with antimicrobial resistance. Int. J. Gen. Med., 11: 25-32.
Pizauro, LJL; deAlmeida, CC; Silva, SR; MacInnes, JI; Kropinski, AM; Zafalon, LF; de Avila, FA and de Mello Varani, A (2021). Genomic comparisons and phylogenetic analysis of mastitis-related staphylococci with a focus on adhesion, biofilm, and related regulatory genes. Sci. Rep., 11: 1-10. https://doi.org/10.1038/s41598-021-96842-2.
Pluta, A; Albritton, LM; Rola-Łuszczak, M and Kuźmak, J (2018). Computational analysis of envelope glycoproteins from diverse geographical isolates of bovine leukemia virus identifies highly conserved peptide motifs. Retrovirology. 15: 1-13. https://doi.org/10.1186/S12977-017-0383-0.
Pond, SLK; Posada, D; Gravenor, MB; Woelk, CH and Frost, SD (2006). Automated phylogenetic detection of recombination using a genetic algorithm. Mol. Biol. Evol., 23: 1891-1901. https://doi.org/10.1093/molbev/msl051.
Ran, W; Kristensen, DM and Koonin, EV (2014). Coupling between protein level selection and codon usage optimization in the evolution of bacteria and archaea. MBio., 5: 1-11.
Rasheed, H; Ijaz, M; Muzammil, I; Ahmed, A; Anwaar, F; Javed, MU; Ghumman, NZ and Raza, A (2023). Molecular evidence of β-lactam resistant Staphylococcus aureus in equids with respiratory tract infections: Frequency and resistance modulation strategy. Acta Tropica. 245: 106967.
Sau, K; Gupta, SK; Sau, S and Ghosh, TC (2005). Synonymous codon usage bias in 16 Staphylococcus aureus phages: implication in phage therapy. Virus Res., 113: 123-131. https://doi.org/10.1016/j.virusres.2005.05. 001. Seo, YS; Lee, DY; Rayamahji, N; Kang, ML and Yoo, HS (2008). Biofilm-forming associated genotypic and phenotypic characteristics of Staphylococcus spp. isolated from animals and air. Res. Vet. Sci., 85: 433-438. https://doi.org/10.1016/j.rvsc.2008.01.005.
Sharp, PM; Bailes, E; Grocock, RJ; Peden, JF and Sockett, RE (2005). Variation in the strength of selected codon usage bias among bacteria. Nucleic Acids Res., 33: 1141-1153. https://doi.org/10.1093/nar/gki242.
Sharp, PM and Cowe, E (1991). Synonymous codon usage in Saccharomyces cerevisiae. Yeast. 7: 657-678. https://doi. org/10.1002/yea.320070702.
Sheppard, S; Guttman, D and Genetics, JFNR (2018). Population genomics of bacterial host adaptation. Nat. Rev. Genet., 19: 549-565.
Shin, HJ; Yang, S and Lim, Y (2021). Antibiotic susceptibility of Staphylococcus aureus with different degrees of biofilm formation. J. Anal. Sci. Technol., 12: 1-7. https://doi.org/10.1186/s40543-021-00294-2.
Suzuki, H; Lefébure, T; Bitar, PP and Stanhope, MJ (2012). Comparative genomic analysis of the genus Staphylococcus including Staphylococcus aureus and its newly described sister species Staphylococcus simiae. BMC Genom., 13: 1-8.
Tamura, K; Peterson, D; Peterson, N; Stecher, G; Nei, M and Kumar, S (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol., 28: 2731-2739. https://doi.org/10.1093/molbev/ msr121.
Thiran, E; DiCiccio, PA; Graber, HU; Zanardi, E; Ianieri, A and Hummerjohann, J (2018). Biofilm formation of Staphylococcus aureus dairy isolates representing different genotypes. J. Dairy Sci., 101: 1000-1012. https://doi.org/ 10.3168/jds.2017-13696.
Vasudevan, P; Nair, MKM; Annamalai, T and Venkitanarayanan, KS (2003). Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation. Vet. Microbiol., 92: 179-185. https://doi.org/10.1016/S0378-1135(02)00360-7.
Wakabayashi, Y; Takemoto, K; Iwasaki, S; Yajima, T; Kido, A; Yamauchi, A; Kuroiwa, K; Kumai, Y; Yoshihara, S; Tokumoto, H and Kawatsu, K (2022). Isolation and characterization of Staphylococcus argenteus strains from retail foods and slaughterhouses in Japan. Int. J. Food Microbiol., 363: 109503.
Wang, Z; Yu, C; Peng, Y; Ding, C; Li, Q; Wang, D and Yuan, X (2019). Close evolutionary relationship between rice black-streaked dwarf virus and southern rice black-streaked dwarf virus based on analysis of their bicistronic RNAs. Virol. J., 16: 1-9. https://doi.org/10.1186/s12985-019-1163-3.
Wiśniewska, K; Garbacz, K and Piechowicz, L (2008). Genotypic screening of atypical Staphylococcus aureus strains isolated from clinical samples for presence of selected adhesin genes. Med. Mal. Infect., 38: 549-553. https://doi.org/10.1016/j.medmal.2008.06.003.
Yang, B; Lei, Z; Zhao, Y; Ahmed, S; Wang, C; Zhang, S; Fu, S; Cao, J and Qiu, Y (2017). Combination susceptibility testing of common antimicrobials in vitro and the effects of Sub-MIC of antimicrobials on Staphylococcus aureus biofilm formation. Front. Microbiol., 8: 1-14. https://doi.org/10.3389/fmicb.2017. 02125. | ||
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