Heavy metal accumulation and changes in soil enzymes activities and bacterial functional diversity under long-term treated wastewater irrigation in East Central region of Tunisia (Monastir governorate)
Introduction
Numerous factors such as the global increase of human development, climate change and pollution are rapidly changing our planet (DeFries et al., 2004; Hagmann et al., 2015). Consequently, the world is facing a serious problem on natural resources availability such as freshwater resources (Pouyat et al., 2007). Thus, various alternatives were developed in order to decrease pressure on natural resources. Besides, the South Mediterranean region which are facing severe water problems, were mandatory searching for alternatives to satisfy their demand especially for agricultural sector (Del Mar Alguacil et al., 2012).
Treated wastewater (TWW) coming from treatment plants is considered as a sustainable alternative increasingly used for various purpose around the world such as land irrigation, decorative fountains, landscape impoundments and groundwater recharge (Pedersen et al., 2003; Levine et Asano, 2004; Wade Miller, 2006; Xu et al., 2010; Adrover et al., 2012). Therefore, TWW irrigation is now recognized as an important supplement of water which also has both positive and negative consequences. It could provide the soil nutrients and organic matter (Jiménez-Cisneros, 1995; Horswell et al., 2003; Rattan et al., 2005). Also, they serve as an environmentally safe disposal method for treated effluents (Ternes et al., 2007; Gwenzi and Munondo, 2008). Therefore, soil that act as filters of toxic chemicals, may adsorb and retain heavy metals, xenobiotics, pathogens, etc. which could be present in TWW. Therefore, numerous recent studies have shown that long-term application of TWW could lead to the accumulation of heavy metals, pharmaceuticals and organic emergent pollutants in the ecosystems receiving secondary TWW (Klay et al., 2010; Bedbabis et al., 2014, 2015; Balkhair and Ashraf, 2016; Houda et al., 2016; Vanryckeghem et al., 2018; Eckert et al., 2018).
Because of its geographical position, Tunisia faces two climates, the Mediterranean in the North and the Saharan in the South generating a spatio-temporal variability of water resources. This situation makes Tunisia a country with low renewable resources which is relatively rare and irregular. Meanwhile, agriculture is typically considered as one of the fields that requires huge amount of water to satisfy demands (Qadir et al., 2010). For this purposes, in 1975 the Tunisian authorities have legalized the reuse of TWW for agricultural, industrial and other purposes. Then, in cooperation with international organization such as FAO, WHO OECD, etc. the national institute of normalization has required severe criteria and limits for better use of non-conventional water resources (Norm 106.02 and 106.03, 1989).
Therefore, there is an increasing interest on the effect of TWW on soils which comes through studying changes in physical, chemical and biological activities in soils in order to understand and to improve the performance of this alternative on crop production and soil fertility (Pedrero et al., 2010; Paudel et al., 2018; Carlos et al., 2018).
On the other hand, while it’s known that TWW are a good way to replace freshwater resources in agriculture and as a natural fertilizer, few studies have already assessed the impact of these non-conventional water on soil’s microbial communities and their activities (Chen et al., 2008; Hidri et al., 2014; Ibekwe et al., 2018). The soil is a key natural resource interacting with above-ground plant and animal communities and contributing to a better functioning (Kennedy and Smith, 2016). Soil quality consists of the chemical, physical and biological components of a soil and their interactions (Arshad and Coen, 1992). Indeed, microbial communities in the soils were known for their significant roles in the nutrients degradation and in the maintaining of soil’s structure (Alexander, 1977; Paul and Clark, 1989). In addition, soil microbial biomass is a fundamental link in the biogeochemical cycles and for the cycling of organic compounds which ensures eventually soil biofertility.
Interestingly, it is well admitted that enzymes in soils coming essentially from bacteria and fungi are involved in the biogeochemical cycles of C, N, P, and S, Therefore, evaluation of their activities could reflect the extent of chemical, pollutants and biological reactions in soils (Dick, 1997; Killham and Staddon, 2002; Chen et al., 2008). In fact, soil enzyme activities changes could provide interesting information on the ability of soils to perform biogeochemical reactions and the impact of anthropogenic and agricultural practices on its composition and health.
In the light of this introduction, this study aims to evaluate microbial properties of five soils sampled from Ouardanin perimeter in the East Central region of Tunisia (Monastir governorate). First, seven enzyme’s activities were assessed. Second, microbial biomass and functional diversity using Biolog Ecoplate™ were evaluated.
Section snippets
Site description and soil sampling
From the East Central region of Tunisia (latitude 35°43 ‘N, longitude 10°40′ E), we have chosen to work on the perimeter of Ouardanin at Monastir Governorate. The air temperatures varied slightly between 17 °C and 29 °C and the annual rainfall range from 270 to 400 mm.
The studied perimeter receive about 3000 m3 TWW.ha−1.year−1 using drip irrigation system. The area covers almost 50 ha and the major vegetation is fruit and olive trees. The samples were taken from five placements noted S1 to S5
Heavy metal contents in soils
The total concentrations of Cd, Cu, Zn, Cr and Ni are displayed in Table 2. For Cd and Cr, there was no significant difference in the trace elements content of S2, S3 and S4 comparing to reference soil S1. Moreover, under 20 years of TWW irrigation, Cu, Zn and Ni concentration increased significantly in the case of S4 samples to reach respectively 23.81 ± 2.22, 19.32 ± 1.38 and 5.81 ± 0.26 ppm. Also, all heavy metals tested in S5 were significantly different compared to S1 and their
Discussion
Soil biofertility is commonly defined as the ability of soils to ensure better plant growth and good quality of vegetables at harvesting (Doran and Zeiss, 2000; Blanco and Lal, 2009). However, soil biofertility involves numerous inputs such as microorganisms, earthworms and plants ensuring through their activities the good functioning of soils. So, under environmental and anthropic pressures, soils component may be exposed to different kind of pollutants such as heavy metals, emergent organic
Conclusion
In conclusion, TWW may contain a variety of components that could enhance bacterial processes in soils. Also, long-term application of these water could modify the functional diversity of microbial communities. On one hand and based on our findings, we can conclude that the long-term TWW reuse in the context of the studied area may represent an interesting alternative to face water shortage in arid regions. On the other hand, it is suggested that risk assessment should be conducted prior to
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This work was supported by funds from the “Ministry of High Education and Scientific Research”. Also, this study was undertaken using facilities in the research unit UR04A6R05 “Laboratory of Biochemistry and Environmental Toxicology” at ISA-CM, Tunisia and the Laboratory of Water, Environment and Urban systems at UPEC, Paris, France.
References (92)
- et al.
Chemical properties and biological activity in soils of Mallorca following twenty years of treated wastewater irrigation
J. Environ. Manage.
(2012) - et al.
Changes in the level of alkaline and acid phosphatase activities during green wastes and sewage sludge co-composting
Bioresour. Technol.
(2010) - et al.
A physiological method for the quantitative measurement of microbial biomass in soils
Soil Biol. Biochem.
(1978) - et al.
Field accumulation risks of heavy metals in soil and vegetable crop irrigated with sewage water in western region of Saudi Arabia
Saudi J. Biol. Sci.
(2016) - et al.
Effect of irrigation with treated wastewater on soil chemical properties and infiltration rate
J. Environ. Manage.
(2014) - et al.
Long-terms effects of irrigation with treated municipal wastewater on soil, yield and olive oil quality
Agric. Water Manag.
(2015) - et al.
Interactions between crop residue and soil organic matter quality and the functional diversity of soil microbial communities
Soil Biol. Biochem.
(2002) - et al.
At environmental doses, dietary methylmercury inhibits mitochondrial energy metabolism in skeletal muscles of the zebra fish (Danio rerio)
INT. J. BIOCHEM. CELL. B.
(2009) - et al.
A novel application of TPAD-MBR system to the pilot treatment of chemical synthesis-based pharmaceutical wastewater
Water Res.
(2008) - et al.
Impact of reclaimed water irrigation on soil health in urban green areas
Chemosphere
(2015)
Effects of olive mill wastewater spreading on the physico-chemical and microbiological characteristics of soil
Int. Biodeterior. Biodegrad.
Toxicity of heavy metals to soil bacteria
FEMS Microbiol. Lett.
Microplastics increase impact of treated wastewater on freshwater microbial community
Environ. Pollut.
Prolonged irrigation with municipal wastewater promotes a persistent and active soil microbial community in a semiarid agroecosystem
Agric. Water Manag.
Effect of cultivation and experimental conditions on the surface reactivity of the metal-resistant bacteria Cupriavidus metallidurans CH34 to protons, cadmium and zinc
Chem. Geol.
Effect of metal contamination on microbial enzymatic activity in soil
Soil Biol. Biochem.
Effects of mercury on soil microbial communities in tropical soils of French Guyana
Appl. Soil Ecol.
Soil moisture pre-treatment effects on enzyme activities as indicators of heavy metal-contaminated and reclaimed soils
Soil Biol. Biochem.
Bio-indicators to assess impacts of heavy metals in land-applied sewage sludge
Soil Biol. Biochem.
Impact of treated wastewater for irrigation on soil microbial communities
Sci. Total Environ.
Wastewater reuse to increase soil productivity
Water Sci. Technol.
Manure biochar influence upon soil properties, phosphorus distribution and phosphatase activities: a microcosm incubation study
Chemosphere
Community level physiological profiles of bacterial communities inhabiting uranium mining impacted sites
Ecotoxicol. Environ. Saf.
Effects of untreated and treated wastewater irrigation on some chemical properties of cauliflower (Brassica olerecea L. var. botrytis) and red cabbage (Brassica olerecea L. var. rubra) grown on calcareous soil in Turkey
Agric. Water Manag.
Effect of irrigation with treated wastewater on geochemical properties (saltiness, C, N and heavy metals) of isohumic soils (Zaouit Sousse perimeter, Oriental Tunisia)
Desalination
A rapid procedure to evaluate the dehydrogenase activity of soils low in organic matter
Soil Biol. Biochem.
Soil heavy metal concentrations, microbial biomass and enzyme activities in a contaminated grassland ecosystem
Soil Biol. Biochem.
Arylsulfatase activity of soil microbial biomass along a Mediterranean-arid transect
Soil Biol. Biochem.
Partial root-zone irrigation enhanced soil enzyme activities and water use of maize under different ratios of inorganic to organic nitrogen fertilizers
Ag. water Manag.
Short-term effects in soil microbial community following agronomic application of olive mill wastewaters in a field of olive trees
Appl. Soil Ecol.
Change in soil properties and the soil microbial community following land spreading of olive mill wastewater affects olive trees key physiological parameters and the abundance of arbuscular mycorrhizal fungi
Soil Biol. Biochem.
Effect of treated wastewater irrigation in East Central region of Tunisia (Monastir governorate) on the biochemical and transcriptomic response of earthworms Eisenia andrei
Sci. Total Environ.
Soil microbial biomass, functional microbial diversity, and nematode community structure as affected by cover crops and compost in an organic vegetable production system
Appl. Soil Ecol.
Treated wastewater irrigation: soil variables and grapefruit tree performance
Agric. Water Manag.
Use of treated municipal wastewater in irrigated agriculture-review of some practices in Spain and Greece
Agric. Water Manag.
Long-term impact of irrigation with sewage effluents on heavy metal content in soils, crops and groundwater - a case study
Agric. Ecosyst. Environ.
Effects of waste water irrigation on soil properties and soil fauna of spinach fields in a West African urban vegetable production system
Environ. Pollut.
Comparison of microbial numbers and enzymatic activities in surface soils and subsoils using various techniques
Soil Biol. Biochem.
Effects of different green manures on soil biological properties and maize yield
Bioresour. Technol.
Irrigation of treated wastewater in Braunschweig, Germany: an option to remove pharmaceuticals and musk fragrances
Chemosphere
Integrated concepts in water reuse: managing global water needs
Desalination
Impact of long-term reclaimed wastewater irrigation on agricultural soils: a preliminary assessment
J. Hazard. Mater.
Functional diversity of microbial communities: a quantitative approach
Soil Biol. Biochem.
Introduction to soil Microbiology
Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties
Soil respiration
Characterization of soil quality: physical and chemical criteria
Am. J. Altern. Agric.
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