Study of the Physicochemical Properties of Streptomyces Cell Surface and their Relationship with Soil Salinity of Origin

• Autorzy: Zanane Chorouk , Mazigh Doha , Mitro Soukaina , Hakim Taoufik , Lekchiri Souad , El Othmany Rabha , El Louali Mostafa , Latrache Hassan , Zahir Hafida

Identyfikatory

DOI

10.12912/27197050/191117

• Języki publikacji: EN

Abstrakty

EN

Physicochemical properties of the bacterial surface are involved in several interfacial phenomena, such as microbial adhesion. Ecology Soil salinity is a crucial parameter for the distribution of Streptomyces. The objective of this study was to investigate the impact of NaCl on the hydrophobicity and electron donor/acceptor characteristics of the cell surface of fourteen Streptomyces strains isolated from soils of the Beni Amir region (Morocco) with different salinities. The physicochemical properties of the surface were evaluated using the MATS (microbial adhesion to solvents) method at two concentrations of NaCl (0.1 M and 1.2 M). The results obtained show a significant change from hydrophilic to hydrophobic character. In particular, the Streptomyces lilaceus A53 strain showed the lowest variation (4.21%). On the other hand, the Streptomyces albogriseolus A65 strain presented the greatest variation (86.15%). These changes were observed when the salt concentration increased significantly from 0.1 M to 1.2 M NaCl. The electron donor/acceptor character systematically decreases and even becomes null for the majority of strains. Furthermore, a strong correlation between cell surface hydrophobicity and salinity of the original soil was observed with MATS at 1.2 M NaCl. This study highlighted the crucial importance of the NaCl concentration in the modulation of the physicochemical properties of the surface of Streptomyces bacteria.

Słowa kluczowe

EN

Streptomyces; hydrophobicity; electron donor properties; electron acceptor properties; soil salinity; MATS method; NaCl concentration

• Wydawca: Lubelski Oddział Polskiego Towarzystwo Inżynierii Ekologicznej ; Lublin University of Technology ; WNGB Wydawnictwo Naukowe
• Czasopismo: Ecological Engineering & Environmental Technology
• Rocznik: 2024
• Tom: Vol. 25, iss. 10
• Strony: 31--43
• Opis fizyczny: Bibliogr. 60 poz., rys., tab.

Twórcy

autor

Zanane Chorouk

• Laboratory of Industrial and Surface Engineering, Bioprocesses and Biointerfaces Team, Faculty of Science and Techniques, Sultan Moulay Slimane University, PO BOX 523 Beni Mellal, Morocco

• https://orcid.org/0000-0002-6334-5386

autor

Mazigh Doha

• Laboratory of Industrial and Surface Engineering, Bioprocesses and Biointerfaces Team, Faculty of Science and Techniques, Sultan Moulay Slimane University, PO BOX 523 Beni Mellal, Morocco

• https://orcid.org/0000-0001-6285-0172

autor

Mitro Soukaina

• Laboratory of Industrial and Surface Engineering, Bioprocesses and Biointerfaces Team, Faculty of Science and Techniques, Sultan Moulay Slimane University, PO BOX 523 Beni Mellal, Morocco

• https://orcid.org/0000-0003-0049-5165

autor

Hakim Taoufik

• Laboratory of Industrial and Surface Engineering, Bioprocesses and Biointerfaces Team, Faculty of Science and Techniques, Sultan Moulay Slimane University, PO BOX 523 Beni Mellal, Morocco

• https://orcid.org/0000-0002-2229-9205

autor

Lekchiri Souad

• Laboratory of Industrial and Surface Engineering, Bioprocesses and Biointerfaces Team, Faculty of Science and Techniques, Sultan Moulay Slimane University, PO BOX 523 Beni Mellal, Morocco

• https://orcid.org/0000-0002-9517-2512

autor

El Othmany Rabha

• Laboratory of Industrial and Surface Engineering, Bioprocesses and Biointerfaces Team, Faculty of Science and Techniques, Sultan Moulay Slimane University, PO BOX 523 Beni Mellal, Morocco

• https://orcid.org/0000-0003-3813-6512

autor

El Louali Mostafa

• Laboratory of Industrial and Surface Engineering, Bioprocesses and Biointerfaces Team, Faculty of Science and Techniques, Sultan Moulay Slimane University, PO BOX 523 Beni Mellal, Morocco

• https://orcid.org/0000-0002-1337-885X

autor

Latrache Hassan

• Laboratory of Industrial and Surface Engineering, Bioprocesses and Biointerfaces Team, Faculty of Science and Techniques, Sultan Moulay Slimane University, PO BOX 523 Beni Mellal, Morocco

• https://orcid.org/0000-0003-2297-9320

autor

Zahir Hafida

• Laboratory of Industrial and Surface Engineering, Bioprocesses and Biointerfaces Team, Faculty of Science and Techniques, Sultan Moulay Slimane University, PO BOX 523 Beni Mellal, Morocco

• https://orcid.org/0000-0001-8663-1775

Bibliografia

• 1. Abdelshafy Mohamad, O.A., Li, L., Ma, J.-B., Hatab, S., Rasulov, B.A., Musa, Z., Liu, Y.-H., Li, W.-J. 2018. Halophilic Actinobacteria Biological Activity and Potential Applications. Microorganisms for Sustainability, 333–364. https://doi.org/10.1007/978-981-13-0329-6_12
• 2. Quba, A.A.A., Goebel, M.-O., Karagulyan, M., Miltner, A., Kästner, M., Bachmann, J., Schaumann, G.E., Diehl, D. 2022. Changes in cell surface properties of Pseudomonas fluorescens by adaptation to NaCl induced hypertonic stress. FEMS Microbes, 4. https://doi.org/10.1093/femsmc/xtac028
• 3. Assaidi, A., Ellouali, M., Latrache, H., Mabrouki, M., Hamadi, F., Timinouni, M., Zahir, H., El Mdaghri, N., Barguigua, A., Mliji, E.M. 2018. Effect of temperature and plumbing materials on biofilm formation by Legionella pneumophilaserogroup 1 and 2–15. Journal of Adhesion Science and Technology, 32(13), 1471–1484. https://doi.org/10.1080/01694243.2018.1423664
• 4. Beck, G., Puchelle, E., Plotkowski, C., Peslin, R. 1988. Effect of growth on surface charge and hydrophobicity of Staphylococcus aureus. Annales de l’Institut Pasteur / Microbiologie, 139(6), 655–664. https://doi.org/10.1016/0769-2609(88)90070-1
• 5. Bellon-Fontaine, M.-N., Rault, J., van Oss, C.J. 1996. Microbial adhesion to solvents: a novel method to determine the electron-donor/electron-acceptor or Lewis acid-base properties of microbial cells. Colloids and Surfaces B: Biointerfaces, 7(1–2), 47–53. https://doi.org/10.1016/0927-7765(96)01272-6
• 6. Bereksi, N., Gavini, F., Benezech, T., Faille, C. 2002. Growth, morphology and surface properties of Listeria monocytogenes Scott A and LO28 under saline and acid environments. Journal of Applied Microbiology, 92(3), 556–565. https://doi.org/10.1046/j.1365-2672.2002.01564.x
• 7. Beroigui, O., Errachidi, F. 2023. Streptomyces at the heart of several sectors to support practical and sustainable applications: A review. Progress In Microbes & Molecular Biology, 6(1). https://doi.org/10.36877/pmmb.a0000345
• 8. Bhatti, A.A., Haq, S., Bhat, R.A. 2017. Actinomycetes benefaction role in soil and plant health. Microbial Pathogenesis, 111, 458–467. https://doi.org/10.1016/j.micpath.2017.09.036
• 9. Bolourian, A., Mojtahedi, Z. 2018. Immunosuppressants produced by Streptomyces: evolution, hygiene hypothesis, tumour rapalog resistance and probiotics. Environmental Microbiology Reports, 10(2), 123–126. Portico. https://doi.org/10.1111/1758-2229.12617
• 10. Boutaleb, N., Latrache, H., Sire, O. 2008. Interactions bactéries-matériaux dans les canalisations d’eau potable. Techniques Sciences Méthodes, 11, 73–90. https://doi.org/10.1051/tsm/200811073
• 11. Bremer, E., Krämer, R. 2019. Responses of microorganisms to osmotic stress. Annual Review of Microbiology, 73(1), 313–334. https://doi.org/10.1146/annurev-micro-020518-115504
• 12. Buzón-Durán, L., Pérez-Lebeña, E., Martín-Gil, J., Sánchez-Báscones, M., Martín-Ramos, P. 2020. Applications of Streptomyces spp. enhanced compost in sustainable agriculture. Biology of Composts, 257– 291. https://doi.org/10.1007/978-3-030-39173-7_13
• 13. Cai, Y., Xue, Q., Chen, Z., Zhang, R. 2009. Classification and salt-tolerance of actinomycetes in the Qinghai Lake Water and lakeside saline soil. Journal of Sustainable Development, 2(1). https://doi.org/10.5539/jsd.v2n1p107
• 14. Claessen, D., Stokroos, I., Deelstra, H.J., Penninga, N.A., Bormann, C., Salas, J.A., Dijkhuizen, L., Wösten, H.A.B. 2004. The formation of the rodlet layer of streptomycetes is the result of the interplay between rodlins and chaplins. Molecular Microbiology, 53(2), 433–443. Portico. https://doi.org/10.1111/j.1365-2958.2004.04143.x
• 15. Costa, O.Y.A., Raaijmakers, J.M., Kuramae, E.E. 2018. Microbial extracellular polymeric substances: ecological function and impact on soil aggregation. Frontiers in Microbiology, 9. https://doi.org/10.3389/fmicb.2018.01636
• 16. De Carvalho, C.C.C.R., Fernandes, P. 2010. Production of metabolites as bacterial responses to the marine environment. Marine Drugs, 8(3), 705–727. https://doi.org/10.3390/md8030705
• 17. De Lima Procópio, R.E., da Silva, I.R., Martins, M.K., de Azevedo, J.L., de Araújo, J.M. 2012. Antibiotics produced by Streptomyces. The Brazilian Journal of Infectious Diseases, 16(5), 466–471. https://doi.org/10.1016/j.bjid.2012.08.014
• 18. Dharmaraj, S. 2010. Marine Streptomyces as a novel source of bioactive substances. World Journal of Microbiology and Biotechnology, 26(12), 2123–2139. https://doi.org/10.1007/s11274-010-0415-613
• 19. Donlan, R.M. 2002. Biofilms: Microbial life on surfaces. Emerging Infectious Diseases, 8(9), 881–890. https://doi.org/10.3201/eid0809.020063
• 20. Dykes, G.A., Sampathkumar, B., Korber, D.R. 2003. Planktonic or biofilm growth affects survival, hydrophobicity and protein expression patterns of a pathogenic Campylobacter jejuni strain. International Journal of Food Microbiology, 89(1), 1–10. https://doi.org/10.1016/s0168-1605(03)00123-5
• 21. EL Othmany, R.E., Zahir, H., Zanane, C., louali, M.E., Latrache, H. 2021. Influence of consistency and composition of growth medium on surface physicochemical properties of Streptomyces. Journal of Pure and Applied Microbiology, 15(3), 1705–1715. https://doi.org/10.22207/jpam.15.3.67
• 22. Elfazazi, K., Zahir, H., Tankiouine, S., Mayoussi, B., Zanane, C., Lekchiri, S., Ellouali, M., Mliji, E.M., Latrache, H. 2021. Adhesion behavior of Escherichia coli strains on glass: Role of cell surface qualitative and quantitative hydrophobicity in their attachment ability. International Journal of Microbiology, 1–9. https://doi.org/10.1155/2021/5580274
• 23. Elgoulli, M., Aitlahbib, O., Tankiouine, S., Assaidi, A., Louali, M.E., Zahir, H., Latrache, H. 2021. The theoretical adhesion of Pseudomonas aeruginosa and Escherichia coli on some plumbing materials in presence of distilled water or tap water. Folia Microbiologica. https://doi.org/10.1007/s12223-021-00868-y
• 24. Elliot, M.A., Karoonuthaisiri, N., Huang, J., Bibb, M.J., Cohen, S.N., Kao, C.M., Buttner, M.J. 2003. The chaplins: a family of hydrophobic cell-surface proteins involved in aerial mycelium formation in Streptomyces coelicolor. Genes & Development, 17(14), 1727–1740. https://doi.org/10.1101/gad.264403
• 25. Gaboriaud, F., Dague, E., Bailet, S., Jorand, F., Duval, J., Thomas, F. 2006. Multiscale dynamics of the cell envelope of Shewanella putrefaciens as a response to pH change. Colloids and Surfaces B: Biointerfaces, 52(2), 108–116. https://doi.org/10.1016/j.colsurfb.2006.04.017
• 26. Gallardo-Moreno, A.M., González-Martín, M.L., Bruque, J.M., Pérez-Giraldo, C., Sánchez-Silos, R., Gómez-García, A.C. 2003. Influence of the growth medium, suspending liquid and measurement temperature on the physico-chemical surface properties of two enterococci strains. Journal of Adhesion Science and Technology, 17(14), 1877–1887. https://doi.org/10.1163/156856103770572034
• 27. Habimana, O., Semião, A.J.C., Casey, E. 2014. The role of cell-surface interactions in bacterial initial adhesion and consequent biofilm formation on nanofiltration/reverse osmosis membranes. Journal of Membrane Science, 454, 82–96. https://doi.org/10.1016/j.memsci.2013.11.043
• 28. Hamadi, F., Latrache, H., Zahir, H., Abed, S.E., Ellouali, M., Saad, I. koraichi. 2012. The relation between the surface chemical composition of Escherichia coli and their electron donor/electron acceptor (Acid-base) properties. Research Journal of Microbiology, 7(1), 32–40. https://doi.org/10.3923/jm.2012.32.40
• 29. Hamadi, F., Latrache, H., Zahir, H., Bengourram, J., Kouider, N., Elghmari, A., Habbari, K. 2011. Evaluation of the relative cell surface charge by using microbial adhesion to hydrocarbon. Microbiology, 80(4), 488–491. https://doi.org/10.1134/s0026261711040072
• 30. Hamadi, F., Latrache, H., Zahir, H., Elghmari, A., Timinouni, M., Ellouali, M. 2008. The relation between Escherichia coli surface functional groups’ composition and their physicochemical properties. Brazilian Journal of Microbiology, 39(1), 10–15. https://doi.org/10.1590/s1517-83822008000100003
• 31. Han, F., Zhang, M., Liu, Z., Shang, H., Li, Q., Zhou, W. 2021. Dynamic characteristics of microbial community and soluble microbial products in partial nitrification biofilm system developed from marine sediments treating high salinity wastewater. Journal of Environmental Management, 290, 112586. https://doi.org/10.1016/j.jenvman.2021.112586
• 32. Kerbab, S. 2018. Actinomycetes in saline soil: the role of natural osmoprotectants.
• 33. Kis-Papo, T., Oren, A., Wasser, S.P., Nevo, E. 2003. Survival of filamentous fungi in hypersaline dead sea water. Microbial Ecology, 45(2), 183–190. https://doi.org/10.1007/s00248-002-3006-8
• 34. Koubali, H., EL Louali, M., Zahir, H., Soufiani, S., Mabrouki, M., Latrache, H. 2021. Physicochemical characterization of glass and polyethylene surfaces treated with different surfactants and their effects on bacterial adhesion. International Journal of Adhesion and Adhesives, 104, 102754. https://doi.org/10.1016/j.ijadhadh.2020.102754
• 35. Krasowska, A., Sigler, K. 2014. How microorganisms use hydrophobicity and what does this mean for human needs? Frontiers in Cellular and Infection Microbiology, 4. https://doi.org/10.3389/fcimb.2014.00112
• 36. Krepsky, N., Ferreira, R.B.R., Nunes, A.P.F., Lins, U.G.C., Filho, F.C. e S., Mattos-Guaraldi, A.L. de, Netto-dosSantos, K.R. 2003. Cell surface hydrophobicity and slime production of Staphylococcus epidermidis Brazilian isolates. Current Microbiology, 46(4), 280–286. https://doi.org/10.1007/s00284-002-3868-5
• 37. Latrache, H. 2001. Physico-chemical study of the cell surface of Escheridia coli: Relationship between the chemical composition of the cell surface and the physico-chemical properties of E. coli.
• 38. Latrache, H., Mozes, N., Pelletier, C., Bourlioux, P. 1994. Chemical and physicochemical properties of Escherichia coli: variations among three strains and influence of culture conditions. Colloids and Surfaces B: Biointerfaces, 2(1–3), 47–56. https://doi.org/10.1016/0927-7765(94)80017-0
• 39. Li, Z., Kawamura, Y., Shida, O., Yamagata, S., Deguchi, T., Ezaki, T. 2002. Bacillus okuhidensis sp. nov., isolated from the Okuhida spa area of Japan. International Journal of Systematic and Evolutionary Microbiology, 52(4), 1205–1209. https://doi.org/10.1099/00207713-52-4-1205
• 40. Maataoui, H., Barkai, H., Sadiki, M., Haggoud, A., Ibnsouda Koraichi, S., Elabed, S. 2014. Physicochemical characterization of actinomycetes isolated from decayed cedar wood: contact angle measurement. Journal of Adhesion Science and Technology, 28(20), 2046– 2053. https://doi.org/10.1080/01694243.2014.943341
• 41. Naïtali, M., Dubois-Brissonnet, F., Cuvelier, G., Bellon-Fontaine, M.-N. 2009. Effects of pH and oilin-water emulsions on growth and physicochemical cell surface properties of Listeria monocytogenes: Impact on tolerance to the bactericidal activity of disinfectants. International Journal of Food Microbiology, 130(2), 101–107. https://doi.org/10.1016/j.ijfoodmicro.2009.01.008
• 42. Oliveira, R., Azeredo, J., Teixeira, P., Fonseca, A.P. 2001. The role of hydrophobicity in bacterial adhesion.
• 43. Pagedar, A., Singh, J., Batish, V.K. 2010. Surface hydrophobicity, nutritional contents affect Staphylococcus aureus biofilms and temperature influences its survival in preformed biofilms. Journal of Basic Microbiology, 50(S1). https://doi.org/10.1002/jobm.201000034
• 44. Petrovicˇ, U., Gunde‐Cimerman, N., Plemenitasˇ, A. 2002. Cellular responses to environmental salinity in the halophilic black yeast Hortaea werneckii. Molecular Microbiology, 45(3), 665–672. https://doi.org/10.1046/j.1365-2958.2002.03021.x
• 45. Roberts, M.F. 2005. Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Systems, 1(1). https://doi.org/10.1186/1746-1448-1-5
• 46. Sarma, S.D. 2001. Spintronics: A new class of device based on electron spin, rather than on charge, may yield the next generation of microelectronics. American Scientist, 89, 516–523.
• 47. Sivalingam, P., Hong, K., Pote, J., Prabakar, K. 2019. Extreme Environment Streptomyces: Potential Sources for New Antibacterial and Anticancer Drug Leads? International Journal of Microbiology, 1–20. https://doi.org/10.1155/2019/5283948
• 48. Song, F., Koo, H., Ren, D. 2015. Effects of material properties on bacterial adhesion and biofilm formation. Journal of Dental Research, 94(8), 1027–1034. https://doi.org/10.1177/0022034515587690
• 49. Van der Wal, A., Norde, W., Zehnder, A.J.B., Lyklema, J. 1997. Determination of the total charge in the cell walls of Gram-positive bacteria. Colloids and Surfaces B: Biointerfaces, 9(1–2), 81–100. https://doi.org/10.1016/s0927-7765(96)01340-9
• 50. Van Dissel, D., Willemse, J., Zacchetti, B., Claessen, D., Pier, G.B., van Wezel, G.P. 2018. Production of poly-β-1,6-N-acetylglucosamine by MatAB is required for hyphal aggregation and hydrophilic surface adhesion by Streptomyces. Microbial Cell, 5(6), 269–279. https://doi.org/10.15698/mic2018.06.635
• 51. Van Elsas, J.D., Adjie Pratama, A., Luis de Araújo, W., Trevors, J.T. 2019. Microbial interactions in soil. Modern Soil Microbiology, 141–161. https://doi.org/10.1201/9780429059186-9
• 52. Xu, H., Zou, Y., Lee, H., Ahn, J. 2010. Effect of NaCl on the biofilm formation by foodborne pathogens. Journal of Food Science, 75(9). Portico. https://doi.org/10.1111/j.1750-3841.2010.01865.x
• 53. Yaradoddi, J.S., Kontro, M.H., Banapurmath, N.R., Ganachari, S.V., Sulochana, M.B., Hungund, B.S., Kazi, Z.K., Anilkumar, S.K., Oli, A. 2021. Extremophilic actinobacteria. Rhizosphere Biology, 55–67. https://doi.org/10.1007/978-981-16-3353-9_4
• 54. Yasuhiro, K., Tieko, Y., Hideo, H. 1972. Alteration of the phospholipid composition of Staphylococcus aureus cultured in medium containing NaCl. Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism, 280(3), 444–450. https://doi.org/10.1016/0005-2760(72)90251-2
• 55. Zabala, D., Braña, A.F., Flórez, A.B., Salas, J.A., Méndez, C. 2013. Engineering precursor metabolite pools for increasing production of antitumor mithramycins in Streptomyces argillaceus. Metabolic Engineering, 20, 187–197. https://doi.org/10.1016/j.ymben.2013.10.002
• 56. Zahir, H., Hamadi, F., Mallouki, B., Imziln, B., Latrache, H. 2016. Effect of salinity on the adhesive power actinomycetes in soil. Journal of Materials and Environmental Science, 7, 3327–3333.
• 57. Zanane, C., Latrache, H., Elfazazi, K., Zahir, H., Ellouali, M. 2018a. Isolation of actinomycetes from different soils of Beni Amir Morocco. J. Mater. Environ. Sci, 9(10), 2994–3000.
• 58. Zanane, C., Mitro, S., Mazigh, D., Lekchiri, S., Hakim, T., El Louali, M., Latrache, H., Zahir, H. 2023. Characterization of Streptomyces Cell Surface by the Microbial Adhesion to Solvents Method. International Journal of Microbiology, 1–8. https://doi.org/10.1155/2023/8841509
• 59. Zanane, C., Zahir, H., Latrache, H., Duponnois, R., Ferhout, H., Elfazazi, K., Ellouali, M. 2018b. Screening of Actinomycetes Isolated from the Soils of the Beni Amir Region of Morocco by the 16S Sequencing of the RDNA Gene.” International Journal of Scientific & Engineering Research 9(5):2363–68.
• 60. Zerva, A., Simić, S., Topakas, E., Nikodinovic-Runic, J. 2019. Applications of Microbial Laccases: Patent Review of the Past Decade (2009–2019). Catalysts, 9(12), 1023. https://doi.org/10.3390/catal9121023