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Prevalence, phenotypic and genotypic diversity, antibiotic resistance, and frequency of virulence genes in Pseudomonas aeruginosa isolated from shrimps

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Abstract

Preventive measures should be prioritized for the increased growth of bacterial contamination in aquatic organisms. This study is aimed at molecular investigation of the prevalence of Pseudomonas aeruginosa, antibiotic resistance, and virulence factor encoding genes. After confirmation of P. aeruginosa collected from shrimp samples (in the same size) in Isfahan and Chabahar (Iran) in summer and autumn, antibiotic resistance encoding genes, virulence factor encoding genes, and multi-drug resistance (MDR) patterns were assessed. Bacterial contamination from Isfahan was higher than Chabahar despite having a cooler climate on summer days. Antibiotic resistance to piperacillin in fresh shrimp samples in summer in Isfahan was contrary to its usage as a front-line antibiotic agent. Lowered MDR pattern in frozen shrimp viability of bacteria was related to the varied expression of antibiotic resistance, highlighting the importance of regulations for cold chain in storage, transportation, and distribution of marine samples compared to fresh shrimps. Foodborne pathogens are of clinical and environmental importance. Results of our study indicated a high rate of frequency for P. aeruginosa isolated from marine samples. Maintenance of cold chain has indispensable roles in preservation, and reduction of P. aeruginosa frequency in aquatic organisms.

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Fig. 1
Fig. 2
Fig. 3

taken from A fresh shrimp and B frozen shrimps. C Results for general comparing of frozen and fresh shrimps

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References

  • Abbas HA, El-Ganiny AM, Kamel HA (2018) Phenotypic and genotypic detection of antibiotic resistance of Pseudomonas aeruginosa isolated from urinary tract infections. Afr Health Sci 18(1):11–21

    Article  PubMed  PubMed Central  Google Scholar 

  • Abd El Tawab AA, Maarouf AA, Ahmed NM (2016) Detection of virulence factors of Pseudomonas species isolated from fresh water fish by PCR. Benha Vet Med J 30(1):199–207

    Article  Google Scholar 

  • Ahari H et al (2020) Evaluation of a multiplex polymerase chain reaction for the simultaneous detection of Vibrio spp. in vegetables and water. Iran J Vet Med 14(4):386–392

    Google Scholar 

  • Ahari H et al (2021) Use of real-time PCR and high-resolution melting analysis for detection and discrimination of Salmonella typhimurium and Salmonella enteritidis in contaminated raw-egg samples. J Food Biosci Technol 11(1):59–68

    Google Scholar 

  • Albuquerque Costa R et al (2015) Antibiotic-resistant Vibrios in farmed shrimp. BioMed Res Int 2015

  • Algammal AM et al (2020) Emerging MDR-Pseudomonas aeruginosa in fish commonly harbor opr L and tox A virulence genes and bla TEM, bla CTX-M, and tet A antibiotic-resistance genes. Sci Rep 10(1):1–12

    Article  Google Scholar 

  • Baquero F, Martínez J-L, Cantón R (2008) Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol 19(3):260–265

    Article  CAS  PubMed  Google Scholar 

  • Barria C, Malecki M, Arraiano C (2013) Bacterial adaptation to cold. Microbiology 159(Pt_12):2437–2443

    Article  CAS  PubMed  Google Scholar 

  • Benie CKD et al (2017) Characterization of virulence potential of Pseudomonas aeruginosa isolated from bovine meat, fresh fish, and smoked fish. Eur J Microbiol Immunol 7(1):55–64

    Article  CAS  Google Scholar 

  • Beshiru A, Igbinosa IH, Igbinosa EO (2019) Prevalence of antimicrobial resistance and virulence gene elements of Salmonella serovars from ready-to-eat (RTE) shrimps. Front Microbiol 10:1613

    Article  PubMed  PubMed Central  Google Scholar 

  • Boss R, Overesch G, Baumgartner A (2016) Antimicrobial resistance of Escherichia coli, Enterococci, Pseudomonas aeruginosa, and Staphylococcus aureus from raw fish and seafood imported into Switzerland. J Food Prot 79(7):1240–1246

    Article  CAS  PubMed  Google Scholar 

  • Brzozowski M et al (2020) Genotypic characterisation and antimicrobial resistance of Pseudomonas aeruginosa strains isolated from patients of different hospitals and medical centres in Poland. BMC Infect Dis 20(1):1–9

    Article  Google Scholar 

  • Bush K (2010) CHAPTER 14 - β-Lactam antibiotics: penicillins. In: Finch RG et al (eds) Antibiotic and Chemotherapy (Ninth Edition). W.B. Saunders, London, pp 200–225

    Chapter  Google Scholar 

  • Chegini Z et al (2020) Bacteriophage therapy against Pseudomonas aeruginosa biofilms: a review. Ann Clin Microbiol Antimicrob 19(1):1–17

    Article  Google Scholar 

  • Chika E et al (2017) Prevalence of AmpC β-lactamase-producing pseudomonas aeruginosa isolates from feacal matter of cow. J Microbiol Exp 4(5):00124

    Google Scholar 

  • Clark ED, MacNaughton L (1917) Shrimp: handling, transportation, and uses. US Department of Agriculture

  • Colomer-Lluch M, Jofre J, Muniesa M (2011) Antibiotic resistance genes in the bacteriophage DNA fraction of environmental samples. PloS one 6(3):e17549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cunningham-Oakes E et al (2019) Understanding the challenges of non-food industrial product contamination. FEMS Microbiol Lett 366(23):fnaa010

    Article  CAS  PubMed  Google Scholar 

  • De Silva BC et al (2018) Frozen white-leg shrimp (Litopenaeus vannamei) in Korean markets as a source of Aeromonas spp. harboring antibiotic and heavy metal resistance genes. Microbial Drug Resist 24(10):1587–1598

    Article  Google Scholar 

  • Dib AL et al (2018) Isolation, molecular characterization and antimicrobial resistance of enterobacteriaceae isolated from fish and seafood. Food Control 88:54–60

    Article  CAS  Google Scholar 

  • Eriksson S, Hurme R, Rhen M (2002) Low–temperature sensors in bacteria. Philos Trans R Soc Lond Ser B Biol Sci 357(1423):887–893

    Article  CAS  Google Scholar 

  • Erickson M et al (2007) Consumer differentiation, acceptance, and demographic patterns to consumption of six varieties of shrimp. J Aquat Food Prod Technol 15(4):35–51

    Article  Google Scholar 

  • Falodun OI, Ikusika EO (2020) Extended spectrum beta-lactamase and metallo beta-lactamase producing Pseudomonas species isolated from fish pond water in Ibadan, Nigeria. Int J Environ Stud 77(5):865–875

    Article  CAS  Google Scholar 

  • Gardiner BJ et al (2019) Nitrofurantoin and fosfomycin for resistant urinary tract infections: old drugs for emerging problems. Aust Prescr 42(1):14–19

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghazy HA et al (2020) Characterization of Pseudomonas aeruginosa ghost and evaluation of its immune proficiency in Nile tilapia (Oreochromis niloticus). Aquac Int 28(6):2517–2529

    Article  CAS  Google Scholar 

  • Guijarro JA et al (2015) Temperature-dependent expression of virulence genes in fish-pathogenic bacteria. Front Microbiol 6(700)

  • Hancock RE, Speert DP (2000) Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and impact on treatment. Drug Resist Updates 3(4):247–255

    Article  CAS  Google Scholar 

  • Heir E et al (2021) Antibiotic resistance and phylogeny of Pseudomonas spp. isolated over three decades from chicken meat in the Norwegian food chain. Microorganisms 9(2):207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Helsens N et al (2020) Antibiotic resistance genes and bacterial communities of farmed rainbow trout fillets (Oncorhynchus mykiss). Front Microbiol 11:3070

    Article  Google Scholar 

  • Hua K et al (2019) The future of aquatic protein: implications for protein sources in aquaculture diets. One Earth 1(3):316–329

    Article  Google Scholar 

  • Hosu MC et al (2020) Antibiotic resistant gene of Pseudomonas aeruginosa from non-clinical environment: public health implications in Mthatha, Eastern Cape Province, South Africa

  • Huse H et al (2018) Evaluation of oxacillin and cefoxitin disk diffusion and MIC breakpoints established by the Clinical and Laboratory Standards Institute for detection of mecA-mediated oxacillin resistance in Staphylococcus schleiferi. J Clin Microbiol 56(2):e01653-e1717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Igbinosa EO, Beshiru A (2019) Antimicrobial resistance, virulence determinants, and biofilm formation of Enterococcus species from ready-to-eat seafood. Front Microbiol 10:728

    Article  PubMed  PubMed Central  Google Scholar 

  • Igbinosa IH, Beshiru A, Igbinosa EO (2017) Antibiotic resistance profile of Pseudomonas aeruginosa isolated from aquaculture and abattoir environments in urban communities. Asian Pac J Trop Dis 7(1):47–52

    Article  Google Scholar 

  • Javiya VA et al (2008) Antibiotic susceptibility patterns of Pseudomonas aeruginosa at a tertiary care hospital in Gujarat, India. Indian J Pharmacol 40(5):230–234

    Article  PubMed  PubMed Central  Google Scholar 

  • Karami P et al (2019) Molecular characterization of clinical and environmental Pseudomonas aeruginosa isolated in a burn center. Saudi J Biol Sci 26(7):1731–1736

    Article  CAS  PubMed  Google Scholar 

  • Karimi E et al (2020) Antibiotic resistance pattern in Pseudomonas aeruginosa isolated from clinical samples other than burn samples in Iran. Avicenna J Med Biotechnol 13(1):35–41

    Google Scholar 

  • Kato K et al (2001) Survey of antibiotic resistance in Pseudomonas aeruginosa by The Tokyo Johoku Association of Pseudomonas Studies. J Infect Chemother 7(4):258–262

    Article  CAS  PubMed  Google Scholar 

  • Khalifa E, Khallaf M, Hashem M (2016) Molecular study on some virulence and fluoroquinolone resistance genes of Pseudomonas aeruginosa isolated from naturally infected cultured sea bream fish (Sparus aurata) in Egypt. J Infect Dis Prev Med 4(136):2

    Google Scholar 

  • Li K, Zheng J (2014) The research on the risk assessment of aquatic product cold chain based on fuzzy comprehensive evaluation. in 2014 11th International Conference on Fuzzy Systems and Knowledge Discovery (FSKD). IEEE

  • Livermore DM (2002) Multiple mechanisms of antimicrobial resistance in Pseudomonas aeruginosa: our worst nightmare? Clin Infect Dis 34(5):634–640

    Article  CAS  PubMed  Google Scholar 

  • Lohr SL (2019) Sampling: design and analysis. Chapman and Hall/CRC

  • MacFadden DR et al (2018) Antibiotic resistance increases with local temperature. Nat Clim Chang 8(6):510–514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahdavi M et al (2017) Frequency of exoY, exoS, exoT and exoU genes among Pseudomonas aeruginosa Isolated from patients in Tehran hospitals by Multiplex PCR. Iran-J-Med-Microbiol 11(1):9–17

    Google Scholar 

  • Mai-Hoang T-D et al (2021) A novel PCR method for simultaneously detecting Acute hepatopancreatic Necrosis Disease (AHPND) and mutant-AHPND in shrimp. Aquaculture 534:736336

    Article  CAS  Google Scholar 

  • McLaughlin HP, Sue D (2018) Rapid antimicrobial susceptibility testing and β-lactam-induced cell morphology changes of Gram-negative biological threat pathogens by optical screening. BMC Microbiol 18(1):218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neu HC (1988) Bacterial resistance to fluoroquinolones. Rev Infect Dis 10(Suppl 1):S57-63

    Article  CAS  PubMed  Google Scholar 

  • Nguyen HNK et al (2014) Molecular characterization of antibiotic resistance in Pseudomonas and Aeromonas isolates from catfish of the Mekong Delta, Vietnam. Vet Microbiol 171(3–4):397–405

    Article  CAS  PubMed  Google Scholar 

  • Odumosu BT et al (2016) Antibiotic susceptibility pattern and analysis of plasmid profiles of Pseudomonas aeruginosa from human, animal and plant sources. Springerplus 5(1):1–7

    Article  CAS  Google Scholar 

  • Osman KM et al (2021) Nile tilapia (Oreochromis niloticus) as an aquatic vector for Pseudomonas species of medical importance: antibiotic resistance association with biofilm formation, quorum sensing and virulence. Aquaculture 532:736068

    Article  CAS  Google Scholar 

  • Piskernik S et al (2011) Reduction of Campylobacter jejuni by natural antimicrobials in chicken meat-related conditions. Food Control 22(5):718–724

    Article  CAS  Google Scholar 

  • Raja RA et al (2017) Pathogenicity profile of Vibrio parahaemolyticus in farmed Pacific white shrimp, Penaeus Vannamei. Fish Shellfish Immunol 67:368–381

    Article  Google Scholar 

  • Raja RA et al (2017) Prevalence of Vibrio spp. with special reference to Vibrio parahaemolyticus in farmed penaeid shrimp Penaeus vannamei (Boone, 1931) from selected districts of Tamil Nadu, India

  • Raja RA et al (2020) Biosafety, withdrawal and efficacy of anti-parasitic drug emamectin benzoate in Asian Seabass (Lates calcarifer). Aquaculture 525:735335

    Article  Google Scholar 

  • Rajaei S, Kazemi-Pour N, Rokhbakhsh-Zamin F (2017) Frequency of plasmid-mediated quinolone resistance genes among clinical isolates of Pseudomonas aeruginosa in Kerman, Iran. Iran J Med Microbiol 11(3):10–18

    Google Scholar 

  • Ravi A et al (2019) Distribution of antibiotic resistance and virulence factors among the bacteria isolated from diseased Etroplus suratensis. 3 Biotech 9(4):1–10

    Article  Google Scholar 

  • Rehman A, Patrick WM, Lamont IL (2019) Mechanisms of ciprofloxacin resistance in Pseudomonas aeruginosa: new approaches to an old problem. J Med Microbiol 68(1):1–10

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Roldán L et al (2018) Pseudomonas aeruginosa isolates from Spanish children: occurrence in faecal samples, antimicrobial resistance, virulence, and molecular typing. BioMed Res Int 2018

  • Ruiz-Roldán L et al (2020) Antimicrobial resistance and virulence of Pseudomonas spp. among healthy animals: Concern about exolysin ExlA detection. Sci Rep 10(1):1–11

    Article  Google Scholar 

  • Sarria-Guzmán Y et al (2014) Identification of antibiotic resistance cassettes in class 1 integrons in Aeromonas spp strains isolated from fresh fish (Cyprinus carpio L.). Curr Microbiol 68(5):581–586

    Article  PubMed  Google Scholar 

  • Shamovsky I, Nudler E (2008) New insights into the mechanism of heat shock response activation. Cell Mol Life Sci 65(6):855–861

    Article  CAS  PubMed  Google Scholar 

  • Soares GMS et al (2012) Mechanisms of action of systemic antibiotics used in periodontal treatment and mechanisms of bacterial resistance to these drugs. J Appl Oral Sci Rev FOB 20(3):295–309

    Article  CAS  Google Scholar 

  • Sonbol FI et al (2015) Correlation between antibiotic resistance and virulence ofPseudomonas aeruginosa clinical isolates. Turk J Med Sci 45(3):568–577

    Article  CAS  PubMed  Google Scholar 

  • Sood S (2016) Chloramphenicol - a potent armament against multi-drug resistant (MDR) gram negative Bacilli? J Clin Diagn Res 10(2):DC01-DC3

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sugden R, Smith T, Jones R (2000) Cochran’s rule for simple random sampling. J R Stat Soc Ser B (Stat Methodol) 62(4):787–793

    Article  Google Scholar 

  • Taengchaiyaphum S et al (2021) Full genome characterization of Laem Singh virus (LSNV) in shrimp Penaeus monodon. Aquaculture 538:736533

    Article  CAS  Google Scholar 

  • Valero A et al (2016) Risk factors influencing microbial contamination in food service centers

  • Vaiyapuri M et al (2021) Antimicrobial resistance in Vibrios of shrimp aquaculture: Incidence, identification schemes, drivers and mitigation measures. Aquac Res

  • Wamala SP et al (2018) Occurrence and antibiotic susceptibility of fish bacteria isolated from Oreochromis niloticus (Nile tilapia) and Clarias gariepinus (African catfish) in Uganda. Fish Aquat Sci 21(1):1–10

    Article  Google Scholar 

  • Yang Y et al (2017) Prevalence, antibiotic susceptibility and diversity of Vibrio parahaemolyticus isolates in seafood from South China. Front Microbiol 8:2566

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

All of the authors and co-authors who meet the criteria for authorship (according to the journal’s instruction) are mentioned on the title page. All of the authors and co-authors would like to warmly appreciate Dr. Momtaz (laboratory manager of Shahrekord Branch, Islamic Azad University, Shahrekord), Mrs. S. Karimi, and Mr. M. Momeni (laboratory experts of Shahrekord Branch, Islamic Azad University, Shahrekord), for their unsparing and meticulous efforts to accomplish this study.

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All of the authors and co-authors who were listed on the title page greatly helped to the accomplishment of this study with unsparing efforts. Hashemi Dehkordi SM helped to the preparation of the last version of the manuscript, and literature review. He also contributed to conducting an experiment, data curation, designation of images and tables, and final arrangement of the data-making structure of the study. Anvar SA mainly did project supervision and corresponding and verified the manuscript by the definitive approval for submission. He also did academic and grammatical peer revision, designation of methodological strategies, and major conceptualization qualifying. Ahari H did scientific consultations, critical revision of the manuscript for important intellectual content according to the journal's instruction, and designation of methodological strategies. Rahimi E helped with conceptualization, revision, methodology, and revision. Ataee M helped for validation of data, edition, and visualization. All of the authors and co-authors attest to the fact that they have approved the final version of the article, and they have received an electronic copy of the manuscript. Also, they attest to the validity and legitimacy of data, and agreed to submit this manuscript to this journal.

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Correspondence to Seyed Amirali Anvar.

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Dehkordi, S.M.H., Anvar, S.A., Rahimi, E. et al. Prevalence, phenotypic and genotypic diversity, antibiotic resistance, and frequency of virulence genes in Pseudomonas aeruginosa isolated from shrimps. Aquacult Int 30, 131–156 (2022). https://doi.org/10.1007/s10499-021-00798-z

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