Preview

Proceedings of Universities. Applied Chemistry and Biotechnology

Advanced search

Resistance of bacterial biofilms comprising activated sludge microbial communities to physicochemical external factors

https://doi.org/10.21285/achb.1010

EDN: AFVEBZ

Abstract

The study was aimed at evaluating the resistance of Alcaligenes faecalis 2, Achromobacter pulmonis, Paenibacillus odorifer, and Bacillus subtilis biofilms to negative physicochemical external factors during batch culture. The main analyzed parameters included temperature (10 and 50 °С) and pH level (5.0 and 10.0), as well as surfactant (sodium dodecyl sulfate) concentrations of 5, 10, and 50 mg/dm3. At low temperatures (10 °С), the size of Alcaligenes faecalis 2, Achromobacter pulmonis PNOS, and Bacillus subtilis biofilms was found to increase. The Alcaligenes faecalis 2 biofilm was noted to exhibit resistance and metabolic activity under acidic conditions. A pH rise to 10.0 resulted in a higher amount of Bacillus subtilis biofilm. When exposed to sodium dodecyl sulfate solution (5 to 10 mg/dm3), Alcaligenes faecalis 2, Bacillus subtilis, Achromobacter pulmonis PNOS, and Paenibacillus odorifer biofilms were observed to form. In response to the exposure to high sodium dodecyl sulfate concentrations (10 and 50 mg/dm3), the biomass and size of Achromobacter pulmonis PNOS biofilm remained unchanged. Thus, the considered cultures were shown to be stress-resistant to negative external factors, which may contribute to the resistance of microbial cultures to various types of pollutants in treatment technologies.

About the Authors

A. A. Khasanova
Kazan National Research Technological University
Russian Federation

Aigul A. Khasanova, Postgraduate Student

68, Karl Marx St., Kazan, 420015



A. S. Sirotkin
Kazan National Research Technological University
Russian Federation

Aleksandr S. Sirotkin, Dr. Sci. (Engineering), Professor, Head of the Department

68, Karl Marx St., Kazan, 420015



E. V. Perushkina
Kazan National Research Technological University
Russian Federation

Elena V. Perushkina, Cand. Sci. (Engineering), Associate Professor

68, Karl Marx St., Kazan, 420015



References

1. Flemming H.-C., Wingender J., Szewzyk U., Steinberg P., Rice S.A., Kjelleberg S. Biofilms: an emergent form of bacterial life. Nature Reviews Microbiology. 2016;14:563575. DOI: 10.1038/nrmicro.2016.94.

2. Stoodley P., Sauer K., Davies D.G., Costerton J.W. Biofilms as complex differentiated communities. Annual Review of Microbiology. 2002;56:187-209. DOI: 10.1146/ annurev.micro.56.012302.160705.

3. Zhao X., Zhao F., Wang J., Zhong N. Biofilm formation and control strategies of foodborne pathogens: food safety perspectives. RSC Advances. 2017;7(58):36670-36683. DOI: 10.1039/C7RA02497E.

4. Ouidir T., Gabriel B., Chabane Y.N. Overview of multispecies biofilms in different ecosystems: wastewater treatment, soil and oral cavity. Journal of Biotechnology. 2022;350:67-74. DOI: 10.1016/j.jbiotec.2022.03.014.

5. Çam S., Brinkmeyer R. The effects of temperature, pH, and iron on biofilm formation by clinical versus environmental strains of Vibrio vulnificus. Folia Microbiologica. 2020;65:557-566. DOI: 10.1007/s12223-019-00761-9.

6. Zhang X.-S., García-Contreras R., Wood T.K. YcfR (BhsA) influences Escherichia coli biofilm formation through stress response and surface hydrophobicity. Journal of Bacteriology. 2007;189(8):3051-3062. DOI: 10.1128/jb.01832-06.

7. Di Bonaventura G., Stepanović, S., Picciani C., Pompilio A., Piccolomini R. Effect of environmental factors on biofilm formation by clinical Stenotrophomonas maltophilia isolates. Folia Microbiologica. 2007;52(1):86-90. DOI: 10.1007/BF02932144.

8. Bisht K., Moore J.L., Caprioli R.M., Skaar E.P., Wakeman C.A. Impact of temperature-dependent phage expression on Pseudomonas aeruginosa biofilm formation. NPJ Biofilms and Microbiomes. 2021;7:22. DOI: 10.1038/ s41522-021-00194-8.

9. Aonofriesei F. Surfactants’ interplay with biofilm development in Staphylococcus and Candida. Pharmaceutics. 2024;16(5):657. DOI: 10.3390/pharmaceutics16050657.

10. Schreiberová O., Hedbávná P., Čejková A., Jirků V., Masák J. Effect of surfactants on the biofilm of Rhodococcus erythropolis, a potent degrader of aromatic pollutants. New Biotechnology. 2012;30(1):62-68. DOI: 10.1016/j.nbt.2012.04.005.

11. Bjergbæk L.A., Haagensen J.A.J., Reisner A., Molin S., Roslev P. Effect of oxygen and growth medium on in vitro biofilm formation by Escherichia coli. Biofilms. 2006;3(1):1-10. DOI: 10.1017/S1479050507002074.

12. Werner E., Roe F., Bugnicourt A., Franklin M.J., Heydorn A., Molin S., et al. Stratified growth in Pseudomonas aeruginosa biofilms. Applied and Environmental Microbiology. 2004;70(10):6188-6196. DOI: 10.1128/AEM.70.10.6188-6196.2004.

13. Bühler T., Ballestero S., Desai M., Brown M.R. Generation of a reproducible nutrient-depleted biofilm of Escherichia coli and Burkholderia cepacia. Journal of Applied Microbiology. 1998;85(3):457-462. DOI: 10.1046/j.1365-2672.1998.853501.x.

14. Alotaibi G.F., Bukhari M.A. Characterization and evaluation of biofilm formation by Klebsiella pneumoniae MBB9 isolated from epilithic biofilms of the Porter Brook River, Sheffield. Edelweiss Journal of Biomedical Research and Review. 2021;3(1):14-24. DOI: 10.33805/2690-2613.120.

15. Wang C., Lin Q., Yao Y., Xu R., Wu X., Meng F. Achieving simultaneous nitrification, denitrification, and phosphorus removal in pilot-scale flow-through biofilm reactor with low dissolved oxygen concentrations: performance and mechanisms. Bioresource Technology. 2022;358:127373. DOI: 10.1016/j.biortech.2022.127373.

16. Khudhair D.N., Hosseinzadeh M., Zwain H.M., Siadatmousavi S.M., Majdi A., Mojiri A. Upgrading the MBBR process to reduce excess sludge production in activated sludge system treating sewage. Water. 2023;15(3):408. DOI: 10.3390/w15030408.

17. Silva T.P., Alves L., Paixão S.M. Effect of dibenzothiophene and its alkylated derivatives on coupled desulfurization and carotenoid production by Gordonia alkanivorans strain 1B. Journal of Environmental Management. 2020;270:110825. DOI: 10.1016/j.jenvman.2020.110825.

18. Zhou X., Liu H., Fan X., Wang X., Bi X., Cheng L., Huang S., et al. Comparative analysis of bacterial information of biofilms and activated sludge in full-scale MBBR-IFAS systems. Microorganisms. 2024;12(6):1121. DOI: 10.3390/microorganisms12061121.

19. Alisawi H.A.O. Performance of wastewater treatment during variable temperature. Applied Water Science. 2020;10:89. DOI: 10.1007/s13201-020-1171-x.

20. Maal-Bared R. Operational impacts of heavy metals on activated sludge systems: the need for improved monitoring. Environmental Monitoring and Assessment. 2020;192(9):560. DOI: 10.1007/s10661-020-08529-2.

21. Lu F., Huang L., Qian F., Jiang Q., Khan S., Shen P. Resistance of anaerobic activated sludge acclimated by different feeding patterns: response to different stress shocks. Water Science and Technology. 2022;85(10):30233035. DOI: 10.2166/wst.2022.164.

22. Németh A., Ainsworth J., Ravishankar H., Lens P.N.L., Heffernan B. Temperature dependence of nitrification in a membrane-aerated biofilm reactor. Frontiers in Microbiology. 2023;14:1114647. DOI: 10.3389/fmicb.2023.1114647.

23. Li J., Xing X.-H., Wang B.-Z. Characteristics of phosphorus removal from wastewater by biofilm sequencing batch reactor (SBR). Biochemical Engineering Journal. 2003;16:279-285.

24. Demakov V.A., Vasil’ev D.M., Maksimova Y.G., Pavlova Y.A., Ovechkina G.V., Maksimov A.Y. Activated sludge bacteria transforming cyanopyridines and amides of pyridinecarboxylic acids. Mikrobiologiya. 2015;84(3):369378. (In Russian). DOI: 10.7868/S0026365615030039. EDN: TQQVBB.

25. Khasanova A.A., Sirotkin A.S., Perushkina E.V. Study on the ability of activated sludge bacteria to form biofilms in vitro. Proceedings of Universities. Applied Chemistry and Biotechnology. 2024;14(2):207-214. (In Russian). DOI: 10.21285/achb.912. EDN: PCUTZF.

26. Maksimova Yu.G., Sergeeva A.A., Ovechkina G.V., Maksimov A.Yu. Pyridine degradation by suspensions and biofilms of Achromobacter pulmonis PNOS and Burkholderia dolosa BOS strains isolated from activated sludge of sewage treatment plants. Biotekhnologiya. 2020;36(2):86-98. (In Russian). DOI: 10.21519/0234-2758-2020-36-2-86-98. EDN: IYFZFI.

27. Kumar A., Bhunia B., Dasgupta D., Mandal T., Dey A., Datta S., et al. Optimization of culture condition for growth and phenol degradation by Alcaligenes faecalis JF339228 using Taguchi methodology. Desalination and Water Treatment. 2013;51(16-18):3153-3163. DOI: 10.1080/19443994.2012.749021.

28. Vandamme P., Moore E.R.B., Cnockaert M., De Brandt E., Svensson-Stadler L., Houf K., et al. Achromobacter animicus sp. nov., Achromobacter mucicolens sp. nov., Achromobacter pulmonis sp. nov. and Achromobacter spiritinus sp. nov., from human clinical samples. Systematic and Applied Microbiology. 2013;36(1):1-10. DOI: 10.1016/j.syapm.2012.10.003.

29. Deng Z., Chen H., Chen S. Medium optimization for nitrogen fixer Paenibacillus sp. 1-49. Acta Microbiologica Sinica. 2016;56(9):1415-1425.

30. Suwanmanon K., Hsieh P.-C. Isolating Bacillus subtilis and optimizing its fermentative medium for GABA and nattokinase production. CyTA – Journal of Food. 2013;12(3):282-290. DOI: 10.1080/19476337.2013.848472.

31. Maksimova Yu., Bykova Ya., Maksimov A. Functionalization of multi-walled carbon nanotubes changes their antibiofilm and probiofilm effects on environmental bacteria. Microorganisms. 2022;10(8):1627. DOI: 10.3390/microorganisms10081627.

32. Singh P., Srivastava S., Malhotra R., Mathur P. Identification of Candida auris by PCR and assessment of biofilm formation by crystal violet assay. Indian Journal of Medical Microbiology. 2023;46:100421. DOI: 10.1016/j.ijmmb.2023.100421.

33. Mathur T., Singhal S., Khan S., Upadhyay D.J., Fatma T., Rattan A. Detection of biofilm formation among the clinical isolates of Staphylococci: an evaluation of three different screening methods. Indian Journal of Medical Microbiology. 2006;24(1):25-29. DOI: 10.1016/S0255-0857(21)02466-X.

34. Luzak B., Siarkiewicz P., Boncler M. An evaluation of a new high-sensitivity PrestoBlue assay for measuring cell viability and drug cytotoxicity using EA.hy926 endothelial cells. Toxicology in Vitro. 2022;83:105407. DOI: 10.1016/j.tiv.2022.105407.

35. Velkov V.V. New insights into the molecular mechanisms of evolution: stress increases genetic diversity. Molecular Biology. 2022;36:209-215. DOI: 10.1023/A:1015365805383.

36. Moreno Switt A.I., Andrus A.D., Ranieri M.L., Orsi R.H., Ivy R., den Bakker H.C., et al. Genomic comparison of sporeforming bacilli isolated from milk. BMC Genomics. 2014;15:26. DOI: 10.1186/1471-2164-15-26.

37. Asadishad B., Olsson A.L.J., Dusane D.H., Ghoshal S., Tufenkji N. Transport, motility, biofilm forming potential and survival of Bacillus subtilis exposed to cold temperature and freeze–thaw. Water Research. 2014;58:239-247. DOI: 10.1016/j.watres.2014.03.048.

38. Klein W., Weber M.H.W., Marahiel M.A. Cold shock response of Bacillus subtilis: isoleucine-dependent switch in the fatty acid branching pattern for membrane adaptation to low temperatures. Journal of Bacteriology. 1999;181(17):5341-5349. DOI: 10.1128/jb.181.17.5341-5349.1999.

39. Beckering C.L., Steil L., Weber M.H.W., Völker U., Marahiel M.A. Genomewide transcriptional analysis of the cold shock response in Bacillus subtilis. Journal of Bacteriology. 2002;184(22):6395-6402. DOI: 10.1128/jb.184.22.6395-6402.2002.

40. Sriwiriyarat T., Nuchlek P. Effects of pH on extracellular polymeric substances compositions of biofilm in Integrated Fixed Film Activated Sludge process. International Journal of Environmental Science and Technology. 2022;19:73-84. DOI: 10.1007/s13762-021-03316-z.

41. Tahir U., Nawaz S., Khan U.H., Yasmin A. Assessment of biodecolorization potentials of biofilm forming bacteria from two different genera for Mordant Black 11 dye. Bioremediation Journal. 2021;25(3):252-270. DOI: 10.1080/10889868.2021.1911920.

42. Rath S., Palit K., Das S. Variable pH and subsequent change in pCO2 modulates the biofilm formation, synthesis of extracellular polymeric substances, and survivability of a marine bacterium Bacillus stercoris GST-03. Environmental Research. 2022;214:114128. DOI: 10.1016/j.envres.2022.114128.

43. Al-Kahachi R., Al-Asadi S., Ali Z.O., Rampurawala J. Effects of genetic and environmental variables on biofilm development dynamics in Achromobacter mucicolens. Iranian Journal of Microbiology. 2023;15(3):414-424. DOI: 10.18502/ijm.v15i3.12902.

44. Chakraborty I., Bhowmick G.D., Nath D., Khuman C.N., Dubey B.K., Ghangrekar M.M. Removal of sodium dodecyl sulphate from wastewater and its effect on anodic biofilm and performance of microbial fuel cell. International Biodeterioration & Biodegradation. 2021;156:105108. DOI: 10.1016/j.ibiod.2020.105108.

45. Gill S.P., Hunter W.R., Coulson L.E., Banat I.M., Schelker J. Synthetic and biological surfactant effects on freshwater biofilm community composition and metabolic activity. Applied Microbiology and Biotechnology. 2022;106:6847-6859. DOI: 10.1007/s00253-022-12179-4.

46. Fedeila M., Hachaïchi-Sadouk Z., Bautista L.F., Simarro R., Nateche F. Biodegradation of anionic surfactants by Alcaligenes faecalis, Enterobacter cloacae and Serratia marcescens strains isolated from industrial wastewater. Ecotoxicology and Environmental Safety. 2018;163:629635. DOI: 10.1016/j.ecoenv.2018.07.123.

47. Sarioglu O.F., Celebioglu A., Tekinay T., Uyar T. Evaluation of contact time and fiber morphology on bacterial immobilization for development of novel surfactant degrading nanofibrous webs. RSC Advances. 2015;5(124):102750102758. DOI: 10.1039/c5ra20739h.


Review

For citations:


Khasanova A.A., Sirotkin A.S., Perushkina E.V. Resistance of bacterial biofilms comprising activated sludge microbial communities to physicochemical external factors. Proceedings of Universities. Applied Chemistry and Biotechnology. (In Russ.) https://doi.org/10.21285/achb.1010. EDN: AFVEBZ

Views: 37


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 2227-2925 (Print)
ISSN 2500-1558 (Online)