Effects of copper on biofilm formation in strains of the genus Enterococcus isolated from an aquatic ecosystem under anthropogenic stress

Main Article Content

Svetlana S. Uskova
Alina V. Martynova

Abstract

Bacteria of the genus Enterococcus can enter an uncultivated but viable state or form biofilms in order to survive in adverse conditions. A biofilm is a porous and complex structure formed by one or more species of microorganisms, organized into several layers irreversibly attached to a biotic or abiotic surface and enclosed in a matrix consisting of extracellular polymeric substances. The aim of this study is to investigate the effects of copper on biofilm formation in strains of the genus Enterococcus isolated from an aquatic ecosystem under anthropogenic stress. A study of biofilm formation in 30 strains of the genus Enterococcus isolated from anthropogenic aquatic ecosystems from March 10, 2018 to September 24, 2020 revealed that the morphology of biofilms varies depending on the presence of copper, their concentration and the type of enterococci (E. faecalis and E. faecium).

Article Details

How to Cite
Uskova С. С., & Martynova А. В. (2025). Effects of copper on biofilm formation in strains of the genus Enterococcus isolated from an aquatic ecosystem under anthropogenic stress. Bulletin of Perm University. Biology, (2), 196–203. https://doi.org/10.17072/1994-9952-2025-2-196-203
Section
Микробиология
Author Biographies

Svetlana S. Uskova , Far Eastern Federal University, Vladivostok, Russia

postgraduate student of the department of biodiversity and marine bioresources

Alina V. Martynova , Pacific State Medical University of the Ministry of Health of Russia, Vladivostok, Russia

doctor of medical sciences, professor of the department of biodiversity and marine bioresources

References

Бузолева Л.С. Микробиологическая оценка качества природных вод. Владивосток, 2011. 85 с.

Коршенко А.Н. Качество морских вод по гидрохимическим показателям. Ежегодник 2019. М.: Наука, 2020. 281 с. EDN: DGTWWQ.

Марданова А.М. и др. Биопленки: Основные принципы организации и методы исследования. Ка-зань, 2016. 42 с.

Прунтова О.В. Лабораторный практикум по общей микробиологии. М.: Владимир, 2005. 77 с.

Шулькин В.М., Богданова Н.Н., Киселев В.И. Металлы в речных водах Приморского края // Геохи-мия. 2007. Т. 1. С. 79–88. EDN: HYRPHJ.

Ускова С.С., Мартынова А.В. Влияние тяжелых металлов на штаммы рода Enterococcus // Вестник Пермского университета. Сер. Биология. 2024. Вып. 4. С. 390‒400. DOI: 10.17072/1994-9952-2024-4-390-400. EDN: MXMDPF.

Boudarel H. et al. Towards standardized mechanical characterization of microbial biofilms: Analysis and critical review // NPJ Biofilms Microbiomes. 2018. Vol. 4. P. 1–15. DOI: 1038/s41522-018-0062-5.

Gomes I.B., Simoes M., Simoes L.C. Copper surfaces in biofilm control // Nanomaterials. 2020. Vol. 10, № 12. Art. 2491. DOI: 10.3390/nano10122491. EDN: NWKKDA.

Hans M. et al. Physicochemical properties of copper important for its antibacterial activity and develop-ment of a unified model // Biointerphases. 2016. Vol. 11. Art. 018902. DOI: 10.1116/1.4935853. EDN: WTRDVR.

Kaplan J.B. et al. Low levels of β-lactam antibiotics induce extracellular DNA release and biofilm for-mation in Staphylococcus aureus // MBio. 2012. Vol. 3, № 4. P. 1–14. DOI: 10.1128/mbio.00198-12.

Lange A. et al. Silver and copper nanoparticles inhibit biofilm formation by mastitis pathogens // Ani-mals. 2021. Vol. 11, № 7. Art. 1884. DOI: 10.3390/ani11071884. EDN: FRRDXD.

Latorre M. et al. CutC is induced late during copper exposure and can modify intracellular copper con-tent in Enterococcus faecalis // Biochem. Biophys. Res. Commun. 2011. Vol. 406, № 4. P. 633−637. DOI: 10.1016/j.bbrc.2011.02.109.

Li Y. et al. Crystal structure of human copper homeostasis protein CutC reveals a potential copper-binding site // J. Struct. Biol. 2010. Vol. 169, № 3. P. 399−405. DOI: 10.1016/j.jsb.2009.10.012. EDN: NZQIMZ.

Lin H. et al. A subcellular level study of copper speciation reveals the synergistic mechanism of microbial cells and EPS involved in copper binding in bacterial biofilms // Environ. Pollut. 2020. Vol. 263. Art. 114485. DOI: 10.1016/j.envpol.2020.114485. EDN: NDCIMB.

Liu Y. et al. Nanotechnology-based antimicrobials and delivery systems for biofilm-infection control // Chem. Soc. Rev. 2019. Vol. 48. P. 428–446. DOI: 10.1039/c7cs00807d.

Mah T.F.C., O’Toole G.A. Mechanisms of biofilm resistance to antimicrobial agents // Trends Microbiol. 2001. Vol. 9. P. 34–39. DOI: 10.1016/s0966-842x(00)01913-2. EDN: AMCZBT.

Muller D., Medigue C., Koechler S.A. A tale of two oxidation states: Bacterial colonization of arsenic-rich environments // PLoS Genetics. 2007. Vol. 3. Art. 53. DOI: 10.1371/journal.pgen.0030053.

Neely A., Maley M.P. Survival of enterococci and staphylococci on hospital fabrics and plastic // J. Clin. Microbiol. 2000. Vol. 38, № 2. P. 724−726. DOI: 10.1128/JCM.38.2.724-726.2000.

Rabin N. et al. Biofilm formation mechanisms and targets for developing antibiofilm agents // Future Med. Chem. 2015. Vol. 7. P. 493–512. DOI: 10.4155/fmc.15.6.

Skowron K. et al. Prevalence and distribution of VRE (vancomycin resistant enterococci) and VSE (van-comycin susceptible enterococci) strains in the breeding environment // Ann. Agric. Environ. Med. 2016. Vol. 23, № 2. P. 231–236. DOI: 10.5604/12321966.1203882.

Stewart P.S. Mechanisms of antibiotic resistance in bacterial biofilms // Int. J. Med. Microbiol. 2002. Vol. 292. P. 107–113. DOI: 10.1078/1438-4221-00196.

Tacconelli E., Cataldo M.A. Vancomycin-resistant enterococci (VRE): transmission and control // Int. J. Antimicrob. 2008. Vol. 31, № 2. P. 99−106. DOI: 10.1016/j.ijantimicag.2007.08.026. EDN: YAEZVF.

Warnes S.L. et al. Biocidal efficacy of copper alloys against pathogenic enterococci involves degradation of genomic and plasmid DNA // Appl. Environ. Microbiol. 2010. Vol. 76, № 16. P. 5390−5401. DOI: 10.1128/AEM.03050-09. EDN: NYOHXN.

Witte W. Glycopeptide resistant Staphylococcus // J. Vet. Med. B Infect. Dis. Vet. Public Health. 2004. Vol. 51. P. 370−373. DOI: 10.1111/j.1439-0450.2004.00774.x.

Wu X., Santos R.S., Fink-Gremmels J. Cadmium modulates biofilm formation by Staphylococcus epi-dermidis // Int. J. Environ. Res. Pub. Health. 2015. Vol. 12. P. 2878−2894. DOI: 10.3390/ijerph120302878.

Yu H. et al. Ultrasound-involved emerging strategies for controlling foodborne microbial biofilms // Trends Food Sci. Technol. 2020. Vol. 96. P. 91–101. DOI: 10.1016/j.tifs.2019.12.010. EDN: LRZPYK.