Elsevier

Journal of Hazardous Materials

Volume 262, 15 November 2013, Pages 1105-1115
Journal of Hazardous Materials

Arbuscular mycorrhizal fungi in arsenic-contaminated areas in Brazil

https://doi.org/10.1016/j.jhazmat.2012.09.063Get rights and content

Abstract

Arbuscular mycorrhizal fungi (AMF) are ubiquitous and establish important symbiotic relationships with the majority of the plants, even in soils contaminated with arsenic (As). In order to better understand the ecological relationships of these fungi with excess As in soils and their effects on plants in tropical conditions, occurrence and diversity of AMF were evaluated in areas affected by gold mining activity in Minas Gerais State, Brazil. Soils of four areas with different As concentrations (mg dm−3) were sampled: reference Area (10); B1 (subsuperficial layer) (396); barren material (573), and mine waste (1046). Soil sampling was carried out in rainy and dry seasons, including six composite samples per area (n = 24). AMF occurred widespread in all areas, being influenced by As concentrations and sampling periods. A total of 23 species were identified, belonging to the following genus: Acaulospora (10 species), Scutellospora (4 species), Racocetra (3 species), Glomus (4 species), Gigaspora (1 species) and Paraglomus (1 species). The most frequent species occurring in all areas were Paraglomus occultum, Acaulospora morrowiae and Glomus clarum. The predominance of these species indicates their high tolerance to excess As. Although arsenic contamination reduced AMF species richness, presence of host plants tended to counterbalance this reduction.

Highlights

► This study is the first one carried out in Brazil. ► Results show a total of 23 AMF species occurring in As contaminated soils. ► The occurrence of AMF varied according to the sampling periods and As contamination. ► Arsenic contamination reduced AMF species richness but host plant counterbalanced.

Introduction

Human health and ecological risks associated with the presence of toxic elements in the environment depends on the total quantity of trace elements or metals present in the environment, as well as on their toxicity, bioavailability, and bioaccessibility. Many studies carried out in areas close to industrial and ore refining complexes indicate high concentrations of trace elements in the soil, which can affect ecosystems functionality, biodiversity and sustainability and may cause irreversible damage to the chemical, physical and biological properties of the soil [1]. During mining activities, several trace elements such as arsenic (As) are exposed on the surface of soils undergoing alteration, which may cause these elements to enter the food web when they are somehow disseminated in the water and/or in the air [2].

The recovery of soils degraded by As in excess is possible by means of several processes, of which revegetation (or phytotechnology) is the most recommended strategy because of its lower cost and the resulting stabilization of the area [3], [4]. On the other hand, a successful establishment of plant coverage in these conditions requires a diverse and functional microbial community. Representatives of such community that should be considered for their relevance are the arbuscular mycorrhizal fungi (AMF). These organisms establish a mutualistic symbiotic relationship with the majority of the terrestrial plants [5] known as arbuscular mycorrhizae (AM) [6], [7] and for this reason represent integrating part of the microbiota of functionally active soils [8], [9]. The importance of AM relies on their capacity to increase water and nutrients uptake, mainly P, in low-fertility soils [10].

Arsenate is dominant molecular form under aerobic conditions in As contaminated soils. Due to the similarity between arsenate and phosphate, plants may absorb arsenate by means of the phosphate channel, and this may occur via the same transporting agents present in the AMF membranes [11], [12], [13], [14]. It is known that phosphate effectively inhibit the arsenate absorption [15], [16], thus decreasing the effects of As phytotoxicity.

Similarly to the plants, AMF can be affected by high As concentrations [17], [18]. In very degraded soils, the AMF diversity and activity are reduced or sometimes eliminated [8], [19]. Klauberg-Filho et al. [19] evaluated the AMF occurrence and diversity in soils of four locations cultivated with grass species and contaminated with heavy metals as a result of Zn extraction and industrialization. They observed that spore abundance, species richness and increase in species dominance were all inversely related to heavy metal concentration. In England, arsenic mine spoil soils were dominated by species of Glomeraceae and Acaulosporaceae [20].

However, AMF mycorrhizal communities from As contaminated soils have never been evaluated in Brazilian soils. High As concentrations can exert a selective effect on the populations, favoring the dominance of more adapted species, which would have an impact on the vegetation by causing differentiated effects on the plants according to the identity of the isolate or fungus species [21]. This could result in alterations in absorption, accumulation or translocation of As in the plant or a better balanced nutrition [17], [18], [22].

In this paper we tested the hypothesis that As soil contamination decreases AMF species richness and root colonization. Efforts to better understand the ecology of these fungi in soils contaminated by As are needed, mainly when the introduction of more efficient species/isolates is intended with the objective of promoting phytostabilization of the contaminated area [22]. The contribution of AMF to the plants growing in soils contaminated with As is related to various aspects such as diversity, abundance, persistence and efficiency of the populations, which can vary from place to place and as a function of environmental variables, as well as due to the presence of vegetation. Therefore, considering that AMF are important ecosystem components, it become relevant to know the impact of this contamination on the occurrence and diversity of native AMF populations in areas degraded by gold mining, which is object of the present study.

Section snippets

Selected areas and sampling

The study areas are located in the Morro do Ouro in the proximity of the Paracatu municipality, northwestern region of Minas Gerais State, Brazil. The mining operations in Paracatu include an open pit mine that produces the lowest gold grades in the world (0.40 g every ton of ore). The company permanently invests in extraction technologies, thus enabling mining operations in Paracatu and ensuring an annual mean production of up to 15 t.

During gold mining, mineral residues or barren material, the

AMF density and diversity in the field soil samples

Spore abundance in RPPN ranged from 167 to 535 per 50 g soil and these values were significantly higher compared to other areas. No spores were detected in BM and MW areas in the rainy season and in MW area in the dry season. For each area, spore abundance in the dry season was 3–10-fold higher compared to the rainy season (Table 2).

Spore abundance, AMF species richness and diversity indices varied according to the sampling area (Table 2).

A total of 23 AMF species was found, 10 belonging to the

Discussion

This study represents the first survey of AMF community in Brazil comparing species richness in As contaminated soils and adjacent non contaminated native areas. A total of 17 species were recovered in the RPPN and eight were detected in each B1 and BM areas with high As. This means that propagules of AMF are somewhat resistant to As contamination and are able to colonize plants and sporulate. Gonzales-Chaves et al. [20] also found a reasonable diverse community of AMF species occurring in As

Conclusions

The occurrence of arbuscular mycorrhizal fungi (spores and colonization) was verified in soil samples with high As contents, and varied according the sampling periods and As contamination.

A total of 23 species was found: 10 of the genus Acaulospora, four of Scutellospora, three of Racocetra, four of Glomus, one of Gigaspora, and one of Paraglomus. G. clarum, P. occultum and A. morrowiae were the more frequent species in the contaminated areas by As. These three species together with A. mellea

Acknowledgments

This work is part of the first author's thesis for the degree of PhD in Soil Science with a research grant from CNPq. The authors acknowledge the funding of the project by CNPq (grant 577513/2008-7), by FAPEMIG (CAG APQ grant 00118/09, CAG PPM grant 187/09, CAG RDP VALE grant 33/10) and CABRNET (The Foundation for Opportunities in Research and Education Resource). Sidney L. Stürmer (Grant 302667/2009-1), Luiz R. G. Guilherme (Grant 305722/2010-7) and Fatima M S Moreira (grant 304574/2010-4)

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