Arbuscular mycorrhizal fungi modulate the chromium distribution and bioavailability in semi-aquatic habitats

https://doi.org/10.1016/j.cej.2021.129925Get rights and content

Highlights

  • Arbuscular mycorrhizal fungi (AMF) improve the wetland plant tolerance to Cr stress.

  • Cr transformation from roots to shoots decrease in AMF inoculated semi-aquatic habitats.

  • AMF can reduce Cr bioavailability and Cr (VI) concentrations in substrates.

  • AMF beneficial for the reduction of Cr content in water under fluctuating water depth.

Abstract

Arbuscular mycorrhizal fungi (AMF) can improve plant tolerance to heavy metal stress in the terrestrial system. However, the detoxification ability of AMF to heavy metals in aquatic systems remains poorly understood. This study investigated the effects of AMF on chromium (Cr) distribution and bioavailability in semi-aquatic habitats under different water depths. Results showed that AMF increased the Cr accumulation in the roots of Iris pseudacorus by 10.0–20.0%. Conversely, Cr concentrations in the shoots of AMF inoculated I. pseudacorus were 21.7–68.4% lower than those in the non-inoculated controls. Besides, Cr concentrations and mass contents in water were decreased by 34.1–35.3% and 15.4–23.3% under the low Cr stress (5 mg kg−1) with AMF inoculation compare to the non-inoculated treatments, respectively. Moreover, Cr (VI) concentrations in substrates under the Cr contents of 5 mg kg−1 were 27.0–44.0% lower than those under the non-inoculated controls. Meanwhile, AMF reduced the Cr bioavailability in substrates under the fluctuating water depth (water depth of 6–3 cm), with an acid-soluble state of Cr decreased by 4.1–5.6%. Furthermore, AMF also enhanced the biomass, nutrient contents (TC, TN, Ca, Mg, Fe, and Mn) in the I. pseudacorus under the fluctuating water depth. Therefore, it provides a possibility that AMF can be used to remove heavy metals from polluted wastewater by semi-aquatic habitats under fluctuating water depth (e.g. tidal flow constructed wetlands).

Introduction

Heavy metals (e.g. Cu, Pb, Ni, Cd, and Cr) discharged from wastewater are easy to accumulate in soils, sediments as well as in-ground or surface water, which pose a serious threat to aquatic ecosystems, food safety, and human health [1]. Therefore, the removal of heavy metals from wastewater is considered to be a major challenge in the field of water pollution. Many techniques (e.g. reverse osmosis, ion exchange, chemical precipitation, adsorption, electrolysis, and solvent extraction) have been established to treat heavy metal polluted wastewater, which provides effective ways for heavy metals removal [2], [3]. However, the application of these technologies also raises additional concerns, such as high construction and operation costs, high energy consumption, complex maintenance, and a large amount of sludge produced [4]. To reduce the cost of heavy metal processing in wastewater, an environmentally friendly and economical treatment technology is needed.

Phytoremediation is considered as a potentially economical and environmentally friendly method of removing heavy metals, and is particularly attractive for not requiring significant advanced engineering work [5]. Generally, wetland plants (especially macrophytes) represent a suitable tool for heavy metals sequestration and phytoremediation in aquatic habitats (e.g. constructed wetlands (CWs) systems) due to their vigorous growth and high aboveground biomass [6]. Heavy metals can be taken up by roots of wetland plants and could be translocated upwards to the aboveground parts (e.g. shoots, stems, and leaves). Vymazal and Březinová (2016) reported that Zn and Cr accumulated in Phragmites australis shoots represented 48.5% and 38.2% of the annual inflow load in the CWs systems, respectively [7]. In addition, heavy metals can be adsorbed on the fine-grained sediment and organic matter in the filtration bed and could be retained by filtration and deposition in the rhizosphere [8]. Although wetland plants have a positive effect on heavy metal removal in aquatic habitats, their resistance to heavy metal toxicity is limited. Batool and Saleh (2020) reported that the high concentrations of heavy metals in the environment may have toxic effects on plants, thereby affecting the regulation of important ions by plants, and ultimately destroying the comprehensive activities of plants [9]. Therefore, it is necessary to improve the tolerance of wetland plants to heavy metal stress, which beneficial for heavy metal removal in semi-aquatic habitats.

Arbuscular mycorrhizal fungi (AMF) are one of the important rhizosphere microorganisms that can form symbiotic associations with most terrestrial plants [10]. They can improve the terrestrial plant's resistance to biotic and abiotic stresses such as salinity, drought, flooding, emerging pollutants, and heavy metals by promoting the nutrients uptake and antioxidant enzyme activities [11]. Nowadays, numerous studies reported that AMF can also establish symbiosis with the roots of some wetland plants in semi-aquatic and aquatic habitats [12], [13]. Moreover, AMF such as Rhizophagus irregularis, Funneliformis mosseae, Claroideoglomus claroideum can widely exist in real-scale wetland habitats around the world (e.g. USA, China, Mexico, Portugal, and Algeria) [12], [14], [15], [16], [17]. Although AMF can colonize the roots of wetland plants in wetland habitats, some researchers found a decrease in the degree of AMF colonization with the increase of flooding gradients and heavy metal concentrations in aquatic systems [18], [19]. Despite that, Ban et al. (2017) indicated that the AMF colonization of P. australis living in the heavy metal polluted wetland habitats ranged from 7 to 35% [20]. Zheng et al. (2015) demonstrated that AMF inoculation and the variation of water contents were highly significant effects on the P. australis growth, and AMF had protective effects for wetland plants against higher heavy metal concentrations in the aboveground tissues [21]. Our previous studies have also proven that the antioxidant enzyme activities in wetland plants at Cr stress were promoted by AMF inoculation under fluctuating water level [22]. Meanwhile, some studies showed that AMF can increase pollutants (e.g. heavy metals, total organic carbon, phosphate, total nitrogen (TN), and ammonium) removal from wastewater in lab-scale and pilot-scale CWs mainly through promoting the plants' uptake, enhancing microorganisms activities around the rhizosphere, and accumulation in their cells [23], [24], [25]. These studies have indicated AMF had positive effects on wetland plant growth under heavy metal stress in semi-aquatic systems, and it also provides a basis for the application of AMF in wastewater purification in real-scale wetland systems. However, the response of wetland plants to heavy metal stress under different water levels is still uncertain regarding various heavy metal concentrations. Furthermore, few studies focus on the effects of AMF on heavy metal distribution and bioavailability in semi-aquatic and aquatic habitats [23], [26].

Therefore, this study aimed to (1) evaluate the effects of AMF on Cr distribution and transformation in semi-aquatic habitats under different water depths; (2) access the response of wetland plants to Cr stress in semi-aquatic habitats under various water depths regarding different Cr concentrations.

Section snippets

Experimental design

The experiment was performed via three Cr levels (0, 5, and 25 mg kg−1 substrate) applied as K2CrO4, two water depths (from bottom to top: 3 cm depth of water, and fluctuating water depth: water depth varies between 3 cm and 6 cm (6–3 cm)), and two AMF treatments (inoculation with AMF and non-inoculation) as three factorial experiments. Each treatment contained three replicates. The period of fluctuating water depth was 4 days (2 days with 3 cm depth of water and 2 days with 6 cm depth of

Effects of Cr and water depth on AMF colonization

The intensities of mycorrhizal colonization (M%) and arbuscule abundance (A%) were gradually decreased with the increase of Cr content under both water depths, and significant differences were obtained between the three Cr treatments (Table 1 and Fig. S2). The intensities of mycorrhizal colonization under both water depths without Cr addition were 10.0–20.4% and 48.5–53.9% higher than those under the Cr contents of 5 mg kg−1 and 25 mg kg−1, respectively. The arbuscule abundance under the

Conclusion

Cr had a negative effect on AMF colonization in wetland plants, especially under high Cr content (25 mg kg−1). Meanwhile, the fluctuating water depth provided a possibility for AMF colonization in the roots of wetland plants. AMF symbiosis improved the tolerance of wetland plants to Cr stress by alleviating the Cr transformation from roots to shoots. Besides, Cr concentrations and contents in water were decreased by AMF inoculation under the fluctuating water depth (water depth of 6–3 cm).

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.

Acknowledgments

This work was financially supported by project IGA (project no. 2020B0031) and complex IGA (support of students for research in the field of natural and constructed wetlands, project no. 42220/1312/3173) of the Faculty of Environmental Sciences, Czech University of Life Sciences Prague. Shanshan Hu would like to thank the China Scholarship Council for the Ph.D. scholarship (CSC, No. 201706760061).

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