Abstract
The effect of wastewater irrigation on the diversity and composition of bacterial communities of soil mesocosms planted with lettuces was studied over an experiment made of five cultivation campaigns. A limited effect of irrigation with either raw or treated wastewater was observed in both α-diversity and β-diversity of soil bacterial communities. However, the irrigation with wastewater fortified with a complex mixture of fourteen relevant chemicals at 10 μg/L each, including pharmaceutical, biocide, and pesticide active substances, led to a drift in the composition of soil bacterial community. One hundred operational taxonomic units (OTUs) were identified as responsible for changes between treated and fortified wastewater irrigation treatments. Our findings indicate that under a realistic agronomical scenario, the irrigation of vegetables with domestic (treated or raw) wastewater has no effect on soil bacterial communities. Nevertheless, under the worst-case scenario tested here (i.e., wastewater fortified with a mixture of chemicals), non-resilient changes were observed suggesting that continuous/repeated irrigation with wastewater could lead to the accumulation of contaminants in soil and induce changes in bacterial communities with unknown functional consequences.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
All the nucleotidic sequences generated in this study have been deposited in the GenBank and are freely available.
References
Balkhair KS (2016) Microbial contamination of vegetable crop and soil profile in arid regions under controlled application of domestic wastewater. Saudi J Biol Sci 23:S83–S92. https://doi.org/10.1016/j.sjbs.2015.10.029
Bender SF, Wagg C, van der Heijden MGA (2016) An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol Evol 31:440–452. https://doi.org/10.1016/j.tree.2016.02.016
Cheng S, Shi M, Xing L, Wang X, Gao H, Sun Y (2020) Sulfamethoxazole affects the microbial composition and antibiotic resistance gene abundance in soil and accumulates in lettuce. Environ Sci Pollut Res 27:29257–29265. https://doi.org/10.1007/s11356-020-08902-1
Cycon M, Borymski S, Zolnierczyk B, Piotrowska-Seget Z (2016) Variable effects of non-steroidal anti-inflammatory drugs (NSAIDs) on selected biochemical processes mediated by soil microorganisms. Front Microbiol 7:1969. https://doi.org/10.3389/fmicb.2016.01969
Delgado-Baquerizo M, Eldridge DJ, Ochoa V, Gozalo B, Singh BK, Maestre FT (2017) Soil microbial communities drive the resistance of ecosystem multifunctionality to global change in drylands across the globe. Ecol Lett 20:1295–1305. https://doi.org/10.1111/ele.12826
Di HJ, Cameron KC, Shen JP, Winefield CS, Ocallaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624. https://doi.org/10.1038/ngeo613
European Comission (2020) Regulation (EU) 2020/741 of the European Parliament and of the Council of 25 May 2020 on minimum requirements for water reuse. Off J Eur Union 2020:32–55
Frenk S, Hadar Y, Minz D (2014) Resilience of soil bacterial community to irrigation with water of different qualities under Mediterranean climate. Environ Microbiol 16:559–569. https://doi.org/10.1111/1462-2920.12183
Gallego S, Martin-Laurent F (2020) Impact of PhACs on Soil Microorganisms, in: Interaction and Fate of Pharmaceuticals in Soil-Crop Systems. In: The Handbook of Environmental Chemistry. Springer, Berlin, Heidelberg, pp 1–44. https://doi.org/10.1007/698_2020_616
Ibekwe AM, Gonzalez-Rubio A, Suarez DL (2018) Impact of treated wastewater for irrigation on soil microbial communities. Sci Total Environ 622–623:1603–1610. https://doi.org/10.1016/j.scitotenv.2017.10.039
Inbar Y (2007) New standards for treated wastewater reuse in Israel, in: NATO Security through Science Series C: Environmental Security. Springer, Dordrecht, pp 291–296. https://doi.org/10.1007/978-1-4020-6027-4_28
ISO 14256-2, 2005. Soil quality—determination of nitrate, nitrite and ammonium in field-moist soils by extraction with potassium chloride solution—Part 2: automated method with segmented flow analysis, International organization for Standardization (ISO).
Leff JW, Jones SE, Prober SM, Barberán A, Borer ET, Firn JL, Harpole WS, Hobbie SE, Hofmockel KS, Knops JMH, McCulley RL, La Pierre K, Risch AC, Seabloom EW, Schütz M, Steenbock C, Stevens CJ, Fierer N (2015) Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad Sci U S A 112:10967–10972. https://doi.org/10.1073/pnas.1508382112
Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24. https://doi.org/10.1890/0012-9615(1999)069[0001:dbratm]2.0.co;2
Manasfi R, Brienza M, Ait-Mouheb N, Montemurro N, Perez S, Chiron S (2020) Impact of long-term irrigation with municipal reclaimed wastewater on the uptake and degradation of organic contaminants in lettuce and leek. Sci Total Environ 765:142742. https://doi.org/10.1016/j.scitotenv.2020.142742
Maron PA, Sarr A, Kaisermann A, Lévêque J, Mathieu O, Guigue J, Karimi B, Bernard L, Dequiedt S, Terrat S, Chabbi A, Ranjard L (2018) High microbial diversity promotes soil ecosystem functioning. Appl Environ Microbiol 84:84. https://doi.org/10.1128/AEM.02738-17
Martin-Laurent F, Topp E, Billet L, Batisson I, Malandain C, Besse-Hoggan P, Morin S, Artigas J, Bonnineau C, Kergoat L, Devers-Lamrani M, Pesce S (2019) Environmental risk assessment of antibiotics in agroecosystems: ecotoxicological effects on aquatic microbial communities and dissemination of antimicrobial resistances and antibiotic biodegradation potential along the soil-water continuum. Environ Sci Pollut Res 26:18930–18937. https://doi.org/10.1007/s11356-019-05122-0
Munoz-Bellido JL, Munoz-Criado S, Garcìa-Rodrìguez JA (2000) Antimicrobial activity of psychotropic drugs. Selective serotonin reuptake inhibitors. Int J Antimicrob Agents 14:177–180. https://doi.org/10.1016/S0924-8579(99)00154-5
Oksanen J, Blanchet FG, Kindt R, Legendre P, McGlinn D, et al. (2019) Vegan: community ecology package. R package version 2.5-5. https://CRAN.R-project.org/package=vegan
Ouyang WY, Su JQ, Richnow HH, Adrian L (2019) Identification of dominant sulfamethoxazole-degraders in pig farm-impacted soil by DNA and protein stable isotope probing. Environ Int 126:118–126. https://doi.org/10.1016/j.envint.2019.02.001
Pedrero F, Kalavrouziotis I, Alarcón JJ, Koukoulakis P, Asano T (2010) Use of treated municipal wastewater in irrigated agriculture-Review of some practices in Spain and Greece. Agric Water Manag 97:1233–1241. https://doi.org/10.1016/j.agwat.2010.03.003
érez Solsona S, Montemurro N, Chiron S, Barceló D, 2021. Interaction and fate of pharmaceuticals in soil-crop systems. The impact of reclaimed wastewater. Pérez Solsona S., Montemurro N., Chiron S., Barceló D. (eds). The Handbook of Environmental Chemistry, vol 103. Springer, Cham. https://doi.org/10.1007/978-3-030-61290-0
Richter E, Wick A, Ternes TA, Coors A (2013) Ecotoxicity of climbazole, a fungicide contained in antidandruff shampoo. Environ Toxicol Chem 32:2816–2825. https://doi.org/10.1002/etc.2367
Romdhane S, Devers-Lamrani M, Beguet J, Bertrand C, Calvayrac C, Salvia M-V, Jrad AB, Dayan FE, Spor A, Barthelmebs L, Martin-Laurent F (2019) Assessment of the ecotoxicological impact of natural and synthetic β-triketone herbicides on the diversity and activity of the soil bacterial community using omic approaches. Sci Total Environ 651:241–249. https://doi.org/10.1016/J.SCITOTENV.2018.09.159
Saccá ML, Barra Caracciolo A, Di Lenola M, Grenni P, 2017. Ecosystem services provided by soil microorganisms, In: Lukac M., Grenni P., Gamboni M. (eds) Soil Biological Communities and Ecosystem Resilience. Sustainability in Plant and Crop Protection. Springer, Cham. https://doi.org/10.1007/978-3-319-63336-7_2
Semedo M, Song B, Sparrer T, Phillips RL (2018) Antibiotic effects on microbial communities responsible for denitrification and N2O production in grassland soils. Front Microbiol 9:2121. https://doi.org/10.3389/fmicb.2018.02121
Solagaistua L, de Guzmán I, Barrado M, Mijangos L, Etxebarria N, García-Baquero G, Larrañaga A, von Schiller D, Elosegi A (2018) Testing wastewater treatment plant effluent effects on microbial and detritivore performance: a combined field and laboratory experiment. Aquat Toxicol 203:159–171. https://doi.org/10.1016/j.aquatox.2018.08.006
Strimmer K (2008) fdrtool: a versatile R package for estimating local and tail area-based false discovery rates. Bioinformatics 24:1461–1462. https://doi.org/10.1093/bioinformatics/btn209
Thelusmond JR, Strathmann TJ, Cupples AM (2016) The identification of carbamazepine biodegrading phylotypes and phylotypes sensitive to carbamazepine exposure in two soil microbial communities. Sci Total Environ 571:1241–1252. https://doi.org/10.1016/j.scitotenv.2016.07.154
Thelusmond JR, Kawka E, Strathmann TJ, Cupples AM (2018) Diclofenac, carbamazepine and triclocarban biodegradation in agricultural soils and the microorganisms and metabolic pathways affected. Sci Total Environ 640–641:1393–1410. https://doi.org/10.1016/j.scitotenv.2018.05.403
Thelusmond JR, Strathmann TJ, Cupples AM (2019) Carbamazepine, triclocarban and triclosan biodegradation and the phylotypes and functional genes associated with xenobiotic degradation in four agricultural soils. Sci Total Environ 657:1138–1149. https://doi.org/10.1016/j.scitotenv.2018.12.145
Valipour M, Singh VP (2016) Global experiences on wastewater irrigation: challenges and prospects. Springer, Cham, pp 289–327. https://doi.org/10.1007/978-3-319-28112-4_18
Van Der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310. https://doi.org/10.1111/j.1461-0248.2007.01139.x
Verhamme DT, Prosser JI, Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J 5:1067–1071. https://doi.org/10.1038/ismej.2010.191
Wagg C, Bender SF, Widmer F, Van Der Heijden MGA (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci U S A 111:5266–5270. https://doi.org/10.1073/pnas.1320054111
Wang S, Gunsch CK (2011) Effects of selected pharmaceutically active compounds on the ammonia oxidizing bacterium Nitrosomonas europaea. Chemosphere 82:565–572. https://doi.org/10.1016/j.chemosphere.2010.10.007
Acknowledgements
We thank Pr Damià Barceló for the coordination of the AWARE project and for scientific discussions.
Funding
This study was financially supported by the EU through the WaterJPI-2015 AWARE project (PCIN-2017-067). The Post-Doc of Dr Sara Gallego was funded by the AWARE project.
Author information
Authors and Affiliations
Contributions
Contribution of each co-author is described below:
Sara Gallego: methodology, validation, formal analysis, investigation, data curation, writing original draft.
Monica Brienza: methodology.
Jérémie Béguet: methodology, data acquisition, and analysis.
Serge Chiron: conceptualization, investigation, writing—review and editing, supervision, project administration, funding acquisition.
Fabrice Martin-Laurent: conceptualization, investigation, writing—review and editing, supervision, project administration, funding acquisition.
Corresponding author
Ethics declarations
Ethical approval
This study did not involve human participants, human material, or human data so it does not need ethical approval document.
Consent to participate
All authors have agreed to participate to this study and were participants of the EU project AWARE funded by the Water JPI-2015 program.
Consent for publication
All authors have agreed to be coauthors of this manuscript.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Diane Purchase
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(DOCX 1.38 mb)
Rights and permissions
About this article
Cite this article
Gallego, S., Brienza, M., Béguet, J. et al. Impact of repeated irrigation of lettuce cultures with municipal wastewater on soil bacterial community diversity and composition. Environ Sci Pollut Res 29, 29236–29243 (2022). https://doi.org/10.1007/s11356-021-14734-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-14734-4