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)

https://doi.org/10.1016/j.agwat.2020.106150Get rights and content

Highlights

  • The impact of TWW irrigation for 20 years was investigated.

  • TWW irrigation had led a significant accumulation of heavy metal.

  • Enzymes activities showed a significant variation among soils.

  • Functional diversity of soil microbial communities was enhanced.

Abstract

Climate change and population growth generates a decrease in water availability around the world which can compromise the maintenance of sustainable agriculture. Thus, treated wastewater (TWW) became an alternative to minimize water shortage. However, this may indirectly affect the soil’s microbial properties. In this study different soils irrigated for 0, 1, 8 and 20 years with TWW were sampled and from the east central region of Tunisia. The objective was to investigate its effect on heavy metal accumulation and enzyme activities of β-glucosidase, arylsulfatase, acid phosphatase, alkaline phosphatase, urease, dehydrogenase and fluorescein diacetate (FDA). Moreover, carbon microbial biomass (Cmic) using Substrate induced respiration (SIR) technique and microbial functional diversity using Biolog EcoPlate™ were assessed. Our results had shown a crucial decrease of the enzymatic activities in soils that were newly irrigated with TWW, while a crucial increase was recorded in soils exposed to TWW for 20 years. In addition, chemical analysis revealed an important accumulation of heavy metals such as Cd, Cu, Zn and Ni along with the irrigation period, especially in 20 years-irrigated soils with TWW. The assessment of the bacterial functional diversity showed an important change in Average well color development (AWCD) and in diversity index values. Besides, substrate utilization profile revealed a significant variation along with the irrigation periods. In conclusion, long-term TWW irrigation has increased the metabolic activities of the soil’s microorganisms. Meanwhile, traces elements accumulation could pose a serious threat for biological processes in soils and a limiting factor for the reuse of TWW in agriculture.

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)

  • M.G. Di Serio et al.

    Effects of olive mill wastewater spreading on the physico-chemical and microbiological characteristics of soil

    Int. Biodeterior. Biodegrad.

    (2008)
  • T. Duxbury

    Toxicity of heavy metals to soil bacteria

    FEMS Microbiol. Lett.

    (1981)
  • E.M. Eckert et al.

    Microplastics increase impact of treated wastewater on freshwater microbial community

    Environ. Pollut.

    (2018)
  • F. Garcia-Orenes et al.

    Prolonged irrigation with municipal wastewater promotes a persistent and active soil microbial community in a semiarid agroecosystem

    Agric. Water Manag.

    (2015)
  • V. Guiné et al.

    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.

    (2007)
  • D.F. Hagmann et al.

    Effect of metal contamination on microbial enzymatic activity in soil

    Soil Biol. Biochem.

    (2015)
  • J. Harris-Hellal et al.

    Effects of mercury on soil microbial communities in tropical soils of French Guyana

    Appl. Soil Ecol.

    (2009)
  • M.B. Hinojosa et al.

    Soil moisture pre-treatment effects on enzyme activities as indicators of heavy metal-contaminated and reclaimed soils

    Soil Biol. Biochem.

    (2004)
  • J. Horswell et al.

    Bio-indicators to assess impacts of heavy metals in land-applied sewage sludge

    Soil Biol. Biochem.

    (2003)
  • A.M. Ibekwe et al.

    Impact of treated wastewater for irrigation on soil microbial communities

    Sci. Total Environ.

    (2018)
  • B. Jiménez-Cisneros

    Wastewater reuse to increase soil productivity

    Water Sci. Technol.

    (1995)
  • Y. Jin et al.

    Manure biochar influence upon soil properties, phosphorus distribution and phosphatase activities: a microcosm incubation study

    Chemosphere

    (2016)
  • A. Kenarova et al.

    Community level physiological profiles of bacterial communities inhabiting uranium mining impacted sites

    Ecotoxicol. Environ. Saf.

    (2014)
  • F.M. Kiziloglu et al.

    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.

    (2008)
  • S. Klay et al.

    Effect of irrigation with treated wastewater on geochemical properties (saltiness, C, N and heavy metals) of isohumic soils (Zaouit Sousse perimeter, Oriental Tunisia)

    Desalination

    (2010)
  • D.A. Klein et al.

    A rapid procedure to evaluate the dehydrogenase activity of soils low in organic matter

    Soil Biol. Biochem.

    (1971)
  • R.G. Kuperman et al.

    Soil heavy metal concentrations, microbial biomass and enzyme activities in a contaminated grassland ecosystem

    Soil Biol. Biochem.

    (1997)
  • X. Li et al.

    Arylsulfatase activity of soil microbial biomass along a Mediterranean-arid transect

    Soil Biol. Biochem.

    (2003)
  • F. Li et al.

    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.

    (2010)
  • B. Mechri et al.

    Short-term effects in soil microbial community following agronomic application of olive mill wastewaters in a field of olive trees

    Appl. Soil Ecol.

    (2007)
  • B. Mechri et al.

    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.

    (2008)
  • M. Mkhinini et al.

    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.

    (2019)
  • A. Nair et al.

    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.

    (2012)
  • I. Paudel et al.

    Treated wastewater irrigation: soil variables and grapefruit tree performance

    Agric. Water Manag.

    (2018)
  • F. Pedrero et al.

    Use of treated municipal wastewater in irrigated agriculture-review of some practices in Spain and Greece

    Agric. Water Manag.

    (2010)
  • R.K. Rattan et al.

    Long-term impact of irrigation with sewage effluents on heavy metal content in soils, crops and groundwater - a case study

    Agric. Ecosyst. Environ.

    (2005)
  • K. Stenchly et al.

    Effects of waste water irrigation on soil properties and soil fauna of spinach fields in a West African urban vegetable production system

    Environ. Pollut.

    (2017)
  • J.P. Taylor et al.

    Comparison of microbial numbers and enzymatic activities in surface soils and subsoils using various techniques

    Soil Biol. Biochem.

    (2002)
  • M. Tejada et al.

    Effects of different green manures on soil biological properties and maize yield

    Bioresour. Technol.

    (2008)
  • T.A. Ternes et al.

    Irrigation of treated wastewater in Braunschweig, Germany: an option to remove pharmaceuticals and musk fragrances

    Chemosphere

    (2007)
  • G. Wade Miller

    Integrated concepts in water reuse: managing global water needs

    Desalination

    (2006)
  • J. Xu et al.

    Impact of long-term reclaimed wastewater irrigation on agricultural soils: a preliminary assessment

    J. Hazard. Mater.

    (2010)
  • J.C. Zak et al.

    Functional diversity of microbial communities: a quantitative approach

    Soil Biol. Biochem.

    (1994)
  • M. Alexander

    Introduction to soil Microbiology

    (1977)
  • J.P.E. Anderson

    Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties

    Soil respiration

    (1982)
  • M.A. Arshad et al.

    Characterization of soil quality: physical and chemical criteria

    Am. J. Altern. Agric.

    (1992)
  • Cited by (29)

    • Improvement of degraded agricultural soil in an arid zone following short- and long-term treated municipal wastewater application: A case study of Gabes perimeter, Tunisia

      2023, Applied Soil Ecology
      Citation Excerpt :

      Instead, the soil samples at 40–60 cm depth after 7 and 15 years of WWTP application showed a high score by indicating a great improvement in terms of physical, chemical, and microbial parameters. Several studies have found similar results to ours showing a positive effect on physical, chemical, biochemical, and microbiological soil properties after irrigation/fertilization with treated wastewater (Hidri et al., 2021; Mkhinini et al., 2020; Belaid et al., 2019). In addition, a similar study showed that WWTP irrigation caused an increase of pathogenic microorganisms, above the legal limit (WHO, 2006), in the irrigated soils and crops (Lüneberg et al., 2018).

    • Disclosing the ecological implications of heavy metal disturbance on the microbial N-transformation process in the ocean tidal flushing urban estuary

      2022, Ecological Indicators
      Citation Excerpt :

      Especially in areas around estuaries, the tidal current present strong and water depth is shallow, the physical mixing effect occurs frequently under the influence of monsoon, which will easily lead to the resuspension of heavy metals from the bottom sediment to the surface (Park et al., 2020; Fernandes et al., 2019). It had been recorded that the distribution of heavy metals varied greatly with the change of the sediment depth (Marouane et al., 2020). In this study, the vertical distribution of heavy metals was found not homogenous in all stations.

    View all citing articles on Scopus
    View full text