Control of Olive Tuberculosis Trees with Olive Mill Wastewater: Inhibition of Pseudomonas savastanoi Adhesion
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Abstract
This innovative study focused on the threat posed by Pseudomonas savastanoi, the causal agent of olive tuberculosis. This pathogen induces the formation of tumors on the bark and leaves of olive trees, adversely affecting the health of the tree and olive oil production. The objective was to assess the effectiveness of a coating based on olive mill wastewater (OMWW) as a biocontrol agent. Specifically, the study examined its influence on the initial adhesion of P. savastanoi on various olive tree surfaces, including bark and the upper and lower leaf surfaces. The physicochemical characteristics of these surfaces were analyzed by evaluating the contact angle between the bacterial strain and the supports, both before and after treatment with OMWW. The results revealed significant variations in initial bacterial adhesion before treatment, with the lower leaf surface (LSL) showing higher adhesion capacity. However, after treatment with OMWW, initial adhesion decreased by up to 95 %, demonstrating the effectiveness of the coating. Furthermore, OMWW treatment influenced the physicochemical characteristics of all supports, particularly the electron donor character, which significantly reduced initial bacterial adhesion. This underscores the crucial role that surface physicochemical properties play in bacterial interactions, both before and after treatment. These findings provide promising insights for the development of sustainable biocontrol methods aimed at mitigating the impact of olive tuberculosis on the olive oil industry.
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Dias B, Lopes M, Ramôa R, Pereira A S, Belo I. Candida tropicalis as a promising oleaginous yeast for olive mill wastewater bioconversion. Energies. 2021 ; 14(3), 640. Doi:https://doi.org/10.3390/en14030640
Caporaso N, Formisano D, Genovese A. Use of phenolic compounds from olive mill wastewater as valuable ingredients for functional foods. Crit. Rev. Food Sci. Nutr. 2018 ; 58(16), 2829-2841. Doi:https://doi.org/10.1080/10408398.2017.1343797
Mostafa S, El-Hassanin A, Soliman A, Rashad S, El-Chaghaby G. Microalgae growth in effluents from olive oil industry for biomass production and decreasing phenolics content of wastewater. Egypt. J. Aquat. Biol. Fish. 2019 ; 23(1), 359-365. Doi:https://dx.doi.org/10.21608/ejabf.2019.28265
Alaoui I, Zahri A, El Kamari F, El Ghadraoui O, Nekhla H, Goubi A, Assouguem A, Annemer S, Ousaaid D, Harrach A, Farah A. (2023). Olive Mill Pomace Impact on the Phytochemical Content and Antioxidant Activity of Rosmarinus officinalis L. Trop. J. Nat. Prod. Res. 2023 ; 7(10), 4186-4192. Doi:http://www.doi.org/10.26538/tjnpr/v7i10.11
Caballero-Guerrero B, Garrido-Fernandez A, Fermoso F G, Rodríguez-Gutierrez G, Fernández-Prior M Á, Reinhard C, Nyström L, Benítez-Cabello A, Arroyo-López F N. Antimicrobial effects of treated olive mill waste on foodborne pathogens. LWT. 2022 ; 164, 113628. Doi:https://doi.org/10.1016/j.lwt.2022.113628
Russo E, Spallarossa A, Comite A, Pagliero M, Guida P, Belotti V, Caviglia D, Schito A M. Valorization and potential antimicrobial use of olive mill wastewater (OMW) from Italian olive oil production. Antioxidants. 2022 ; 11(5), 903. Doi:https://doi.org/10.3390/antiox11050903
Bouarab-Chibane L, Forquet V, Lantéri P, Clément Y, Léonard-Akkari L, Oulahal N, Degraeve P, Bordes C. Antibacterial properties of polyphenols: characterization and QSAR (Quantitative structure-activity relationship) models. Front. microbiol. 2019 ; 10, 829. Doi:https://doi.org/10.3389/fmicb.2019.00829
Hakim T, Lekchiri S, Latrache H, El Amine Afilal M, Jaafari A, Tankiouine S, Ellouali M, Zahir H. Study of initial adhesion of a bacterium to different support materials before and after conditioning film of olive oil-mill wastewater. Adv Biosci Biotechnol. 2020 ; 11(08), 391-404. Doi:https://doi.org/10.4236/abb.2020.118027
Barguigua A, Zahir I, Youss S, Fikri N, Youss B. Prevalence of olive tree phytopathologies of microbial origin in Fquih Ben Salah, Azilal and Beni Mellal (Morocco). J. Anal. Sci. Appl. Biotec. 2021 ; 3(1), 3-1.
Caballo-Ponce E, Meng X, Uzelac G, Halliday N, Cámara M, Licastro D, Passos da Silva D, Ramos C, Venturi, V. Quorum sensing in Pseudomonas savastanoi pv. savastanoi and Erwinia toletana: role in virulence and interspecies interactions in the olive knot. Appl. Environ. Microbiol. 2018 ; 84(18), e00950-18. Doi:https://doi.org/10.1128/AEM.00950-18
Xie Y, Shao X, Zhang Y, Liu J, Wang T, Zhang W, Hua C, Deng X. Pseudomonas savastanoi two-component system RhpRS switches between virulence and metabolism by tuning phosphorylation state and sensing nutritional conditions. Mbio. 2019 ; 10(2), 10-1128. Doi:https://doi.org/10.1128/mbio.02838-18
Al-Obady G, İlbaş A L İ, Al-Kawthary S. In Vitro Pathogenicity of Pseudomonas savastanoi isolated from Olive Trees in Iraq on Fruits of Various Plant Species and Their Molecular Characterisation. Am. J. Biomed. Res. 2023 ; 19(1). Doi:http://doi.org/10.34297/ajbsr.2023.19.002557
Carniello V, Peterson B W, Van der Mei H C, Busscher H J. Physico-chemistry from initial bacterial adhesion to surface-programmed biofilm growth. Adv. Colloid Interface Sci. 2018 ; 261, 1-14. Doi: https://doi.org/10.1016/j.cis.2018.10.005
Sierra J D M, Oosterkamp M J, Wang W, Spanjers H, Van Lier J B. Comparative performance of upflow anaerobic sludge blanket reactor and anaerobic membrane bioreactor treating phenolic wastewater: Overcoming high salinity. J. Chem. Eng. 2019 ; 366, 480-490. Doi: https://doi.org/10.1016/j.cej.2019.02.097
Zheng S, Bawazir M, Dhall A, Kim H-E, He L, Heo J, Hwang G. Implication of surface properties, bacterial motility, and hydrodynamic conditions on bacterial surface sensing and their initial adhesion. Front. bioeng. biotechnol. 2021 ; 9, 643722. Doi : https://doi.org/10.3389/fbioe.2021.643722
Hamadi F, Asserne F, Elabed S, Bensouda S, Mabrouki M, Latrache, H. Adhesion of Staphylococcus aureus on stainless steel treated with three types of milk. Food Control. 2014 ; 38, 104-108. Doi : https://doi.org/10.1016/j.foodcont.2013.10.006
Hamadi F, Latrach, H, Mabrrouki M, Elghmari A, Outzourhit A, Ellouali M, Chtaini A. Effect of pH on distribution and adhesion of Staphylococcus aureus to glass. J. Adhes. Sci. Technol. 2005 ; 19(1), 73-85. Doi : https://doi.org/10.1163/1568561053066891
Busscher H J, Weerkamp A H, Van der Mei H C, Van Pelt A W, De Jong H P, Arends J. Measurement of the surface free energy of bacterial cell surfaces and its relevance for adhesion. Appl. Environ. Microbiol. 1984 ; 48(5), 980-983. Doi : https://doi.org/10.1128/aem.48.5.980-983.1984
Van Oss C J, Chaudhur M K, Good R J. Interfacial Lifshitz-van der Waals and polar interactions in macroscopic systems. Chem. Rev. 1988 ; 88(6), 927-941. Doi : https://doi.org/10.1021/cr00088a006
Habouzit F, Gévaudan G, Hamelin J, Steyer J-P, Bernet N. Influence of support material properties on the potential selection of Archaea during initial adhesion of a methanogenic consortium. Bioresour. Technol. 2011 ; 102(5), 4054-4060. Doi : https://doi.org/10.1016/j.biortech.2010.12.023
Nguyen V, Karunakaran E, Collins G, Biggs C A. Physicochemical analysis of initial adhesion and biofilm formation of Methanosarcina barkeri on polymer support material. Colloids Surf. B Biointerfaces. 2016 ; 143, 518-525. Doi : https://doi.org/10.1016/j.colsurfb.2016.03.042
Achinas S, Charalampogiannis N, Euverink G J W. A brief recap of microbial adhesion and biofilms. Appl. Sci. 2019 ; 9(14), 2801. Doi:https://doi.org/10.3390/app9142801
Latrache H, El G, Karroua M, Hakkou A, Ait M H, El B, Bourlioux P. Relations between hydrophobicity tested by three methods and surface chemical composition of Escherichia coli. The new microbiologica. 2002 ; 25(1), 75-82.
Cai L, Wu D, Xia J, Shi H, Kim H. Influence of physicochemical surface properties on the adhesion of bacteria onto four types of plastics. Sci. Total Environ. 2019 ; 671, 1101-1107. Doi : https://doi.org/10.1016/j.scitotenv.2019.03.434
Van Oss C J, Chaudhur M K, Good R J. Interfacial Lifshitz-van der Waals and polar interactions in macroscopic systems. Chem. Rev. 1988 ; 88(6), 927-941. Doi : https://doi.org/10.1021/cr00088a006
Van Oss C J. Hydrophobicity of biosurfaces-origin, quantitative determination and interaction energies. Colloids Surf. B. Biointerfaces. 1995 ; 5(3-4), 91-110. Doi : https://doi.org/10.1016/0927-7765(95)01217-7
Morgan-Sagastume F. Biofilm development, activity and the modification of carrier material surface properties in moving-bed biofilm reactors (MBBRs) for wastewater treatment. Crit. Rev. Environ. Sci. Technol. 2018 ; 48(5), 439-470. Doi: https://doi.org/10.1080/10643389.2018.1465759
McEldowney S, Fletcher M. Variability of the influence of physicochemical factors affecting bacterial adhesion to polystyrene substrata. Appl. Environ. Microbiol. 1986 ; 52(3), 460-465. Doi : https://doi.org/10.1128/AEM.52.3.460-465.1986
Pratt-Terpstra I H, Weerkamp A H, Busscher H J. On a relation between interfacial free energy-dependent and noninterfacial free energy-dependent adherence of oral Streptococci to solid substrata. Curr. Microbiol.. 1988 ; 16, 311-313. Doi : https://doi.org/10.1007/BF01568537
Sjollema J, Van der Mei H, Uyen H, Busscher H. The influence of collector and bacterial cell surface properties on the deposition of oral Streptococci in a parallel plate flow cell. J ADHES SCI TECHNOL. 1990 ; 4(1), 765-777. Doi : https://doi.org/10.1163/156856190X00658
Della Volpe C, Siboni S. From van der Waals equation to acid-base theory of surfaces: a chemical-mathematical journey. Rev. Adhes. Adhes. 2022 ; (1), 47-97. Doi: https://dx.doi.org/10.47750/RAA/10.1.02
Tong C Y, Chang Y S, Ooi B S, Chan D J C. Physico-chemistry and adhesion kinetics of algal biofilm on polyethersulfone (PES) membrane with different surface wettability. J. Environ. Chem. Eng. 2021 ; 9(6), 106531. Doi: https://doi.org/10.1016/j.jece.2021.106531
Li Y, Sui J, Cui L S, Jiang H L. Hydrogen bonding regulated flexibility and disorder in hydrazone-linked covalent organic frameworks. J. Am. Chem. Soc. 2023 ; 145(2), 1359-1366. Doi: https://doi.org/10.1021/jacs.2c11926
Bellon-Fontaine M-N, Rault J, Van Oss C. Microbial adhesion to solvents: a novel method to determine the electron-donor/electron-acceptor or Lewis acid-base properties of microbial cells. Colloids Surf. B Biointerfaces. 1996 ; 7(1-2), 47-53. Doi : https://doi.org/10.1016/0927-7765(96)01272-6
Gallardo-Moreno A, González-Martı́n M, Perez-Giraldo C, Bruque J, Gomez-Garcıa A. The measurement temperature: an important factor relating physicochemical and adhesive properties of yeast cells to biomaterials. J. Colloid. Interface. Sci. 2004 ; 271(2), 351-358. Doi : https://doi.org/10.1016/j.jcis.2003.12.008
Thakur B, Zhou G, Chang J, Pu H, Jin B, Sui X, Yuan X, Yang C, Magruder M, Chen J. Rapid detection of single E. coli bacteria using a graphene-based field-effect transistor device. Biosens Bioelectron. 2018 ; 110, 16-22. Doi: https://doi.org/10.1016/j.bios.2018.03.014
Bouhia Y, Hafidi M, Ouhdouch Y, Soulaimani A, Zeroual Y, Lyamlouli, K. Microbial intervention improves pollutant removal and semi-liquid organo-mineral fertilizer production from olive mill wastewater sludge and rock phosphate. J. Environ. Manage. 2024 ; 354, 120317. Doi: https://doi.org/10.1016/j.jenvman.2024.120317
Mozes N, Léonard A, Rouxhet P. G. On the relations between the elemental surface composition of yeasts and bacteria and their charge and hydrophobicity. Biochim. Biophys. Acta. 1988 ; 945(2), 324-334.
Cowan M, Van der Mei H, Rouxhet P, Busscher H. Physico-chemical and structural properties of the surfaces of Peptostreptococcus micros and Streptococcus mitis as compared to those of Mutans streptococci, Streptococcus sanguis and Streptococcus salivarius. Microbiology. 1992 ; 138(12), 2707-2714. Doi : https://doi.org/10.1099/00221287-138-12-2707
Latrache H, Mozes N, Pelletier C, Bourlioux P. Chemical and physicochemical properties of Escherichia coli: variations among three strains and influence of culture conditions. Colloids Surf. B Biointerfaces. 1994 ; 2(1-3), 47-56. Doi : https://doi.org/10.1016/0927-7765(94)80017-0
Van der Mei H, Busscher H. The use of X-ray photoelectron spectroscopy for the study of oral Streptococcal cell surfaces. Adv. Dent. Res. 1997 ; 11(4), 388-394. Doi : https://doi.org/10.1177/08959374970110040301
Van Oss C J. Interfacial forces in aqueous media: CRC press. 2006. Doi : https://doi.org/10.1201/9781420015768
Van oss C V, Good R J, Busscher R J. Estimation of the polar surface tension parameters of glycerol and formamide, for use in contact angle measurements on polar solids. J. Disp. Sci. Tech. 1990 11(1), 75-81. Doi : https://doi.org/10.1080/01932699008943237
Assaidi A, Ellouali M, Latrache H, Mabrouki M, Timinouni M, Zahir H, Tankiouine S, Barguigua A, Mliji E. Adhesion of Legionella pneumophila on glass and plumbing materials commonly used in domestic water systems. Int. J. Environ. Health Res. 2018 ; 28(2), 125-133. Doi : https://doi.org/10.1080/09603123.2018.1429580
Talluri S N, Winter R M, Salem D R. Conditioning film formation and its influence on the initial adhesion and biofilm formation by a Cyanobacterium on photobioreactor materials. Biofouling. 2020 ; 36(2), 183-199. Doi: https://doi.org/10.1080/08927014.2020.1748186
Ugwu C N, Ezeibe E N, Eze C C, Evurani S A, Emencheta S C, Kenechukwu F C, Akpa P A, Attama A A. Anti-bacterial susceptibility and biofilm-forming ability of foodborne pathogens isolated from minimally processed fruits and vegetables obtained from markets in southeastern nigeria. Trop. J. Nat. Prod. Res. 2022 ; 6(3). Doi: http://www.doi.org/10.26538/tjnpr/v1i4.5
Compere C, Bellon‐Fontaine M N, Bertrand P, Costa D, Marcus P, Poleunis C, Pradier C-M, Rondot B, Walls M G. Kinetics of conditioning layer formation on stainless steel immersed in seawater. Biofouling. 2001 ; 17(2), 129-145. Doi : https://doi.org/10.1080/08927010109378472
Poleunis C, Compere C, Bertrand P. Time-of-flight secondary ion mass spectrometry: characterisation of stainless steel surfaces immersed in natural seawater. J. Microbiol. Methods. 2002 ; 48(2-3), 195-205. Doi : https://doi.org/10.1016/S0167-7012(01)00323-2
Poleunis C, Rubio C, Compere C, Bertrand P. ToF–SIMS chemical mapping study of protein adsorption onto stainless steel surfaces immersed in saline aqueous solutions. Appl. Surf. Sci. 2003 ; 203, 693-697.
Paraskeva C, Papadakis V, Tsarouchi E, Kanellopoulou D, Koutsoukos P. Membrane processing for olive mill wastewater fractionation. Desalination. 2007 ; 213(1-3), 218-229. Doi : https://doi.org/10.1016/j.desal.2006.04.087
Van Oss C, Chaudhury M, Good R. The mechanism of phase separation of polymers in organic media-apolar and polar systems. Sep. Sci. Technol. 1989 ; 24(1-2), 15-30. Doi : https://doi.org/10.1080/01496398908049748
Hamadi F, Latrache H, Asserne F, Elabed S, Zahir H, Saad I K, Hanine H, Bengourram J. Quantitative adhesion of Staphylococcus aureus on stainless steel coated with milk. J. Food Sci. Nutr. 2013 ; 4(03), 299. Doi : https://doi.org/10.4236/fns.2013.43040
Rosmaninho R, Santos O, Nylander T, Paulsson M, Beuf M, Benezech T, Yiantsios S, Andritsos N, Karabelas A, Rizzo G, Müller-Steinhagen H, Melo L. Modified stainless steel surfaces targeted to reduce fouling–Evaluation of fouling by milk components. J. Food Eng. 2007 ; 80(4), 1176-1187. Doi : https://doi.org/10.1016/j.jfoodeng.2006.09.008
Van Oss C J, Giese R F, Wu W. On the predominant electron-donicity of polar solid surfaces. J. Adhes. 1997 ; 63(1-3), 71-88. Doi : https://doi.org/10.1080/00218469708015214