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Relation to enterocins of variable Aeromonas species isolated from trouts of Slovakian aquatic sources and detected by MALDI-TOF mass spectrometry

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Abstract

Aeromonads represent bacteria thought to be primarily mostly autochthonous to aquatic environments. This study was focused on the relation with antibiotics and enterocins of identified Aeromonas species isolated from the intestine of trouts living in Slovakian aquatic sources. Intestinal samples from 50 trouts (3 Salmo trutta and 47 Salmo gairdnerii) were collected in April of years 2007, 2010, and 2015 from trouts of different water sources in Slovakia (pond Bukovec near Košice, river Čierny Váh). Due to the MALDI-TOF mass spectrometry evaluation, 25 strains were proposed to the genus Aeromonas involving nine different species (Aeromonas bestiarum—nine strains, Aer. salmonicida—four strains, Aer. encheleia, Aer. eucrenophila, Aer. molluscorum, Aer. media, Aer. sobria, Aer. popoffii, Aer. veronii). Phenotypic evaluation of individual strains confirmed their species identification. Twenty-five strains of different Aeromonas species were sensitive to azithromycin, amikacin, mecillinam, mezlocillin, piperacillin, gentamicin, chloramphenicol, and tetracycline. On the other side, they were resistant to carbenicillin and ticarcillin. The growth of Aer. bestiarum R41/1 was inhibited by treatment with Ent M and Ent 2019 (inhibition activity 100 AU/mL). Aer. bestiarum R47/3 was inhibited by eight enterocins (100 AU/mL). It is the first study testing enterocins to inhibit the growth of Aeromonas species from trouts.

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References

  • Alfaia AJ., Ribeiro MHL, Francisco APG, Alfaia CM, Fraqueza MJ (2015) Bacteriocin microencapsulation: production and application on dry-fermented meat sausages manufacture. Portuguese traditional meat products: strategies to improve safety and quality workshop, Lisbon, 9th of June 2015, p.1–17

  • Borchard MA, Stemper ME, Standridge JH (2003) Aeromonas isolates from human diarrheic stool and groundwater compared by pulsed-field gel electrophoresis. Emerg Infect Dis 9:224–228

    Article  Google Scholar 

  • Bruker Daltonics Biotyper 2.2 (2008) Software for microorganism identification and classification user manual

  • Chhabra S, Durant E, Fish L, Karlyshev A, Macintyre S, Stewart G, Swift S, Williams P, Winson M (1997) Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida. J Bacteriol 177:5271–5281

    Google Scholar 

  • Clinical and Laboratory Standards Institute-CLSI (2011) Performance standards for antimicrobial susceptibility testing; 21st inform. suppl. CLSI document. CLSI, Wayne, pp M100–MS21

    Google Scholar 

  • Dallaire-Dufresne S, Tanaka KH, Trudel MV Lafaille A, Charette SJ (2014) Virulence, genomic features, and plasticity of Aeromonas salmonicida subsp. salmonicida, the causative agent of fish furunculosis. Vet Microbiol 169:1–7. https://doi.org/10.1016/j.vetmic.2013.06.025

    Article  CAS  PubMed  Google Scholar 

  • De Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer KH, Whitman W (2009) In Bergeys manual of systematic bacteriology—second edition. Springer

  • De Vuyst L, Callewaert R, Pot B (1996) Characterization of antagonistic activity of Lactobacillus amylovorus DCE471 and lasrge scale isolation of its bacteriocin amylovorin L471. Syst Appl Microbiol 19:9–20

    Article  Google Scholar 

  • Fečkaninová A, Koščová J, Mudroňová D, Popelka P, Toropilová J (2017) The use of probiotic bacteria against Aeromonas infections in salmonid aquaculture. Aquaculture 469:1–8

    Article  Google Scholar 

  • Graf J (2015) Aeromonas. Caister Academic Press. Springer, New York, ISBN 0-387-95041-9

  • Joseph SW, Carnahan A (1994) The isolation, identification and systematics of the motile Aeromonas species. Annu Rev Fish Dis 4:315–343

    Article  Google Scholar 

  • Karaffová V, Marcinková E, Bobíková K, Herich R, Revajová V, Stašová D, Kavuľová A, Levkutová M, Levkut MJ, Lauková A, Ševčíková Z, MSr L (2017) TLR4 and TLR21 expression, MIF, IFN-β, MD-2, CD14 activation, and sIgA production in chickens administered with EFAL41 strain challenged with Campylobacter jejuni. Folia Microbiol 62:89–97

    Article  CAS  Google Scholar 

  • Lauková A (2001) Effect of enterocins CCM 4231 and V24 on the cells of environmental isolates Acinetobacter spp. Acta Vet Brno 70:473–477

    Article  Google Scholar 

  • Lauková A, Mareková M, Javorský P (1993) Detection and antimicrobial spectrum of a bacteriocin-like substance produced by Enterococcus faecium CCM 4231. Lett Appl Microbiol 16:257–260

    Article  Google Scholar 

  • Lauková A, Guba P, Nemcová R, Mareková M (2004) Inhibition of Salmonella enterica serovar Dusseldorf by enterocin A in gnotobiotic Japanese quails. Vet Med Czech 49:47–51

    Article  Google Scholar 

  • Lauková A, Simonová M, Strompfová V, Štyriak I, Ouwehand AC, Várady M (2008) Potential of enterococci isolated from horses. Anaerobe 14:234–236

    Article  CAS  PubMed  Google Scholar 

  • Lauková A, Szabóová R, Strompfová V, Simonová M, Žitňan R (2009) Sensitivity of Yersinia-like bacteria isolated from fishes to antimicrobials. SL J Food Sci, (Potravinárstvo, in Slovak) 3:28–31

    Google Scholar 

  • Lauková A, Hádryová J, Imrichová J, Strompfová V, Kandričáková A (2012a) Enterococus faecium EM41 isolate from ostriches and its enterocin. Folia Vet 56:34–36

    Google Scholar 

  • Lauková A, Chrastinová Ľ, Pogány Simonová M, Strompfová V, Plachá I, Čobanová K, Formelová Z, Chrenková M, Ondruška Ľ (2012b) Enterococcus faecium AL41:its enterocin M and their beneficial use in rabbits husbandry. Prob Antimic Prot 4:243–249

    Article  Google Scholar 

  • Lauková A, Kandričáková A, Strompfová V, Chacornac JP, Léroy S, Žitňan R (2013) Staphylococcal species detected in free-living trouts of east Slovakian water sources and their relation to antimicrobials. Bul Vet Inst Pulawy 57:167–171

    Article  CAS  Google Scholar 

  • Lauková A, Kandričáková A, Ščerbová J, Szabóová R, Plachá I, Čobanová K, Pogány Simonová M, Strompfová V (2017a) In vivo model experiment using laying hens treated with Enterococcus faecium EM41 from ostrich faeces and its enterocin EM41. Mac Vet Rev 40:157–166

    Article  CAS  Google Scholar 

  • Lauková A, Chrastinová Ľ, Plachá I, Szabóová R, Kandričáková A, Pogány Simonová M, Formelová Z, Ondruška Ľ, Goldová M, Chrenková M, Strompfová V (2017b) Enterocin 55 produced by non rabbit-derived strain Enterococcus faecium EF55 in relation with microbiota and selected parameters in broiler rabbits. Int J Environm Agric Res 3:45–52 ISSN.[4254-1850]

    Google Scholar 

  • Marciňáková M, Lauková A, Simonová M, Strompfová V, Koréneková B, Naď P (2008) A new probiotic and bacteriocin-producing strain of Enterococcus faecium EF9296 and its use in grass ensiling. Czech J Anim Sci 53:336–345

    Article  Google Scholar 

  • Mareková M, Lauková A, De Vuyst L, Skaugen M, Nes IF (2003) Partial characterization of bacteriocins produced by environmental strain Enterococcus faecium EK13. J Appl Microbiol 94:523–530

    Article  PubMed  Google Scholar 

  • Mareková M, Lauková A, Skaugen M, Nes IF (2007) Isolation and characterisation of a new bacteriocin termed enterocin M, produced by enviromental isolate Enterococcus faecium AL 41. J Ind Microbiol Biotechnol 34:533–537

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Cruz P, Ibanéz AL, Monroy hermosillo OA, Ramiréz Saa HC (2012) Use of probiotics in aquaculture. ISRN Microbiology 916845. https://doi.org/10.5402/2012/916845

    Article  Google Scholar 

  • Martínez-Murcia AJ, Monera A, Saavedra MJ, Oncina R, Lopez-Alvarez M, Lara E, Figueras MJ (2011) Multilocus phylogenetic analysis of the genus Aeromonas. Syst Appl Microbiol 34:189–199

    Article  CAS  PubMed  Google Scholar 

  • Petersen A, Dalsgaard A (2003) Antimicrobial resistance of intestinal Aeromonas spp. and Enterococcus spp. in fish cultured in integrated broiler-fish farms in Thailand. Aquaculture 219:395–402

    Article  CAS  Google Scholar 

  • Piotrowska M, Popowska M (2014) The prevalence of antibiotic resistance genes among Aeromonas species in aquatic environments. Ann Microbiol 64:921–934

    Article  CAS  Google Scholar 

  • Pogány Simonová M, Lauková A, Plachá I, Čobanová K, Strompfová V, Szabóová R, Chrastinová Ľ (2013) Can enterocins affect phagocytosis and gluthatione-peroxidase in rabbits? Cent Eur J Biol 8:730–734

    Google Scholar 

  • Shah SQA, Karatas S, Nilsen H, Steinum TM, Colquhoun DJ, Sorum H (2012) Characterization and expression of the gyr A gene from quinolone resistant Yersinia ruckeri strains isolated from Atlantic salmon (Salmo salar L.) in Norway. Aquaculture 350-353:37–41

    Article  CAS  Google Scholar 

  • Strompfová V, Lauková A (2007) In vitro study on bacteriocin of Enterococci associated with chickens. Anaerobe 13:228–237

    Article  CAS  PubMed  Google Scholar 

  • Yanong RPE, Francis-Floyd R (2017) Bacterial diseases in aquaculture. Vet Manual of Merck (on-line)

  • Zhang T, Zhang M, Zhang X, Fang HH (2009) Tetracycline resistance genes and tetracycline resistant lactose-fermenting Enterobacteriacae in activated sludge of sewage treatment plants. Environ Sci Technol 43:3455–3460

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was partially supported by the project VEGA 2/0006/17. We would like to thank for excellent laboratory work Mrs. Margita Bodnárová.

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Correspondence to Andrea Lauková.

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Lauková, A., Kubašová, I., Kandričáková, A. et al. Relation to enterocins of variable Aeromonas species isolated from trouts of Slovakian aquatic sources and detected by MALDI-TOF mass spectrometry. Folia Microbiol 63, 749–755 (2018). https://doi.org/10.1007/s12223-018-0616-1

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