Microbial Bioactives
Microbial Bioactives | Online ISSN 2209-2161
295
Citations
198.7k
Views
157
Articles
REVIEWS (Open Access)
Environmental Dissemination of Antimicrobial Resistance in Olive Cultivation Systems: Insights from Wastewater and Soil Microbiomes
Ahsan Habib 1*
Microbial Bioactives 7 (1) 1-8 https://doi.org/10.25163/microbbioacts.7110663
Submitted: 27 May 2024 Revised: 25 July 2024 Accepted: 05 August 2024 Published: 07 August 2024
Abstract
Antimicrobial resistance (AMR) has emerged as a critical global challenge, extending beyond clinical settings into environmental and agricultural systems. Wastewater treatment plants (WWTPs) act as hotspots for antibiotic-resistant bacteria (ARB) and antibiotic resistance genes (ARGs), driven by residual antibiotics, heavy metals, and high microbial density. When reclaimed wastewater and agro-industrial by-products, such as olive mill wastewater (OMW), are used in olive cultivation, they may introduce resistance determinants into soil and plant microbiomes. Olive trees (Olea europaea L.) harbor complex microbial communities, including arbuscular mycorrhizal fungi (AMF) and plant growth-promoting rhizobacteria (PGPR), which support nutrient cycling, abiotic stress tolerance, and overall plant health. However, anthropogenic pressures from wastewater irrigation, industrial effluents, and agricultural management practices may alter these beneficial communities, promoting persistence and horizontal transfer of ARGs. This systematic review and meta-analysis synthesizes evidence on AMR dissemination from wastewater to olive agroecosystems, examining microbial community shifts, resistance gene prevalence, and environmental factors influencing ARG persistence. Findings indicate that while WWTPs and reclaimed water can enhance soil fertility, they simultaneously pose risks of resistance propagation, particularly when biofilms, co-selective agents, and high microbial densities are present. Integrating microbial community management, sustainable irrigation practices, and advanced wastewater treatment may mitigate AMR risks in agroecosystems. Understanding these interactions is vital for maintaining both environmental and public health, as resistance determinants in soil and crop microbiomes may enter food webs, posing long-term ecological and human health challenges.
Keywords: Antimicrobial resistance; Wastewater treatment; Olive cultivation; Soil microbiome; Arbuscular mycorrhizal fungi; Plant growth-promoting rhizobacteria; Olive mill wastewater
References
Auguet, O., Pijuan, M., Borrego, C. M., Rodriguez-Mozaz, S., Triadó-Margarit, X., Giustina, S. V. D., & Gutierrez, O. (2017). Sewers as potential reservoirs of antibiotic resistance. Science of the Total Environment, 605, 1047–1054. https://doi.org/10.1016/j.scitotenv.2017.06.153
Berendonk, T. U., Manaia, C. M., Merlin, C., Fatta-Kassinos, D., Cytryn, E., Walsh, F., … Norström, M. (2015). Tackling antibiotic resistance: the environmental framework. Nature Reviews Microbiology, 13(5), 310–317. https://doi.org/10.1038/nrmicro3439
Bizos, G., Papatheodorou, E. M., Chatzistathis, T., Ntalli, N., Aschonitis, V. G., & Monokrousos, N. (2020). The role of microbial inoculants on plant protection, growth stimulation, and crop productivity of the olive tree (Olea europea L.). Plants, 9(6), 743. https://doi.org/10.3390/plants9060743
Boukhdoud, N., Gros, R., Darwish, T., & Farnet, A. M. S. (2016). Effect of agricultural practices and coastal constraints on soil microbial functional properties in Mediterranean olive orchards. European Journal of Soil Science, 67(4), 470–477. https://doi.org/10.1111/ejss.12351
Gao, P., He, S., Huang, S., Li, K., Liu, Z., Xue, G., & Sun, W. (2015). Impacts of coexisting antibiotics, antibacterial residues, and heavy metals on the occurrence of erythromycin resistance genes in urban wastewater. Applied Microbiology and Biotechnology, 99(9), 3971–3980. https://doi.org/10.1007/s00253-014-6247-z
Garcia-Barrionuevo, A., Moreno, E., Quevedo-Sarmiento, J., Gonzalez-Lopez, J., & Ramos-Cormenzana, A. (1992). Effect of wastewaters from olive oil mills (Alpechin) on Azotobacter nitrogen fixation in soil. Soil Biology and Biochemistry, 24(3), 281–283. https://doi.org/10.1016/0038-0717(92)90235-K
Maheshwari, M., Ahmad, I., & Althubiani, A. S. (2016). Multidrug resistance and transferability of blaCTX-M among extended-spectrum β-lactamase-producing enteric bacteria in biofilm. Journal of Global Antimicrobial Resistance, 6, 142–149. https://doi.org/10.1016/j.jgar.2016.05.002
Marathe, N. P., Regina, V. R., Walujkar, S. A., Charan, S. S., Moore, E. R., Larsson, D. G., & Shouche, Y. S. (2013). A treatment plant receiving wastewater from multiple bulk drug manufacturers is a reservoir for highly multi-drug resistant integron-bearing bacteria. PLoS ONE, 8(10), e77310. https://doi.org/10.1371/journal.pone.0077310
Mechri, S., Mechri, B., Kharazmi, A., & Mahmoud, O. (2007). Long-term effects of olive mill wastewater application on soil microbial activity and composition. Soil Biology and Biochemistry, 39(6), 1299–1307. https://doi.org/10.1016/j.soilbio.2006.12.040
Melloni, R., & Cardoso, E. J. B. N. (2023). Microbiome associated with olive cultivation: A review. Plants, 12(4), 897. https://doi.org/10.3390/plants12040897
Montes-Borrego, M., Navas-Cortés, J. A., & Landa, B. B. (2013). Linking microbial functional diversity of olive rhizosphere soil to management systems in commercial orchards in southern Spain. Agriculture, Ecosystems & Environment, 181, 169–178. https://doi.org/10.1016/j.agee.2013.09.023
Narciso-da-Rocha, C., Vercammen, K., Thys, S., Van Bergen, M., Roosens, N. H., Demeestere, K., & Dewulf, J. (2018). Impact of wastewater treatment on the abundance of antibiotic resistance genes and their association with mobile genetic elements in effluents. Water Research, 145, 498–508. https://doi.org/10.1016/j.watres.2018.08.006
Nasini, L., Gigliotti, G., Balduccini, M. A., Federici, E., Cenci, G., & Proietti, P. (2013). Effect of solid olive-mill waste amendment on soil fertility and olive (Olea europaea L.) tree activity. Agriculture, Ecosystems & Environment, 164, 292–297. https://doi.org/10.1016/j.agee.2012.10.006
Ouledali, S., Ennajeh, M., Zrig, A., Gianinazzi, S., & Khemira, H. (2018). Estimating the contribution of arbuscular mycorrhizal fungi to drought tolerance of potted olive trees (Olea europaea). Acta Physiologiae Plantarum, 40(5), 81. https://doi.org/10.1007/s11738-018-2656-1
Page, M. J., McKenzie, J. E., Bossuyt, P. M., Boutron, I., Hoffmann, T. C., Mulrow, C. D., Shamseer, L., Tetzlaff, J. M., Akl, E. A., Brennan, S. E., Chou, R., Glanville, J., Grimshaw, J. M., Hróbjartsson, A., Lalu, M. M., Li, T., Loder, E. W., Mayo-Wilson, E., McDonald, S., … Moher, D. (2021). The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ, 372, n71. https://doi.org/10.1136/bmj.n71
Porras-Soriano, A., Soriano-Martin, M. L., Porras-Piedra, A., & Azcón, R. (2009). Arbuscular mycorrhizal fungi increased growth, nutrient uptake, and tolerance to salinity in olive trees under nursery conditions. Journal of Plant Physiology, 166(13), 1350–1359. https://doi.org/10.1016/j.jplph.2009.02.010
Proietti, P., Federici, E., Fidati, L., Scargetta, S., Massaccesi, L., Nasini, L., … Gigliotti, G. (2015). Effects of amendment with oil mill waste and its derived compost on soil chemical and microbiological characteristics and olive (Olea europaea L.) productivity. Agriculture, Ecosystems & Environment, 207, 51–60. https://doi.org/10.1016/j.agee.2015.03.028
Rizzo, L., Manaia, C., Merlin, C., Schwartz, T., Dagot, C., Ploy, M. C., … Fatta-Kassinos, D. (2013). Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Science of the Total Environment, 447, 345–360. https://doi.org/10.1016/j.scitotenv.2013.01.032
Sofo, A., Ciarfaglia, A., Scopa, A., Camele, I., Curci, M., Crecchio, C., … Palese, A. M. (2014). Soil microbial diversity and activity in a Mediterranean olive orchard using sustainable agricultural practices. Soil Use and Management, 30(1), 160–167. https://doi.org/10.1111/sum.12097
Szczepanowski, R., Linke, B., Krahn, I., Gartemann, K. H., Gützkow, T., Eichler, W., … Schlüter, A. (2009). Detection of 140 clinically relevant antibiotic-resistance genes in the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to selected antibiotics. Microbiology, 155(7), 2306–2319. https://doi.org/10.1099/mic.0.028233-0
Tello, A., Austin, B., & Telfer, T. C. (2012). Selective pressure of antibiotic pollution on bacteria of importance to public health. Environmental Health Perspectives, 120(8), 1100–1106. https://doi.org/10.1289/ehp.1104650
Varela, A. R., Nunes, O. C., & Manaia, C. M. (2016). Quinolone-resistant Aeromonas spp. as carriers and potential tracers of acquired antibiotic resistance in hospital and municipal wastewater. Science of the Total Environment, 542, 665–671. https://doi.org/10.1016/j.scitotenv.2015.10.124
Voigt, A. M., Zacharias, N., Timm, C., Wasser, F., Sib, E., Skutlarek, D., … Exner, M. (2020). Association between antibiotic residues, antibiotic resistant bacteria and antibiotic resistance genes in anthropogenic wastewater — An evaluation of clinical influences. Chemosphere, 241, 125032. https://doi.org/10.1016/j.chemosphere.2019.125032
Recommended articles
Yeast-Derived Biomolecules in Green Nanotechnology: Bridging Sustainable Bioeconomy and Early-Life Antimicrobial Resistance Management
Rethinking Antimicrobial Strategies: Integrating Microbiome Modulation and Next-Generation Therapeutics to Combat Multidrug-Resistant Pathogens
Marine Microbial Natural Products as a Frontier in Drug Discovery: A Systematic Review
0
Save
Save
0
Citation
Citation
9
View
View
0
Share
Share