Heavy-Metal Stress and Developmental Patterns of Arbuscular Mycorrhizal Fungi

Abstract

The rate of global deposition of Cd, Pb, and Zn has decreased over the past few decades, but heavy metals already in the soil may be mobilized by local and global changes in soil conditions and exert toxic effects on soil microorganisms. We examined in vitro effects of Cd, Pb, and Zn on critical life stages in metal-sensitive ecotypes of arbuscular mycorrhizal (AM) fungi, including spore germination, presymbiotic hyphal extension, presymbiotic sporulation, symbiotic extraradical mycelium expansion, and symbiotic sporulation. Despite long-term culturing under the same low-metal conditions, two species, Glomus etunicatum and Glomus intraradices, had different levels of sensitivity to metal stress. G. etunicatum was more sensitive to all three metals than was G. intraradices. A unique response of increased presymbiotic hyphal extension occurred in G. intraradices exposed to Cd and Pb. Presymbiotic hyphae of G. intraradices formed presymbiotic spores, whose initiation was more affected by heavy metals than was presymbiotic hyphal extension. In G. intraradices grown in compartmentalized habitats with only a portion of the extraradical mycelium exposed to metal stress, inhibitory effects of elevated metal concentrations on symbiotic mycelial expansion and symbiotic sporulation were limited to the metal-enriched compartment. Symbiotic sporulation was more sensitive to metal exposure than symbiotic mycelium expansion. Patterns exhibited by G. intraradices spore germination, presymbiotic hyphal extension, symbiotic extraradical mycelium expansion, and sporulation under elevated metal concentrations suggest that AM fungi may be able to survive in heavy metal-contaminated environments by using a metal avoidance strategy.Mining and smelting of metalliferous ores combined with combustion of fossil fuels have dramatically increased the global deposition of Cd, Pb, and Zn over the past two centuries (10). This trend has been somewhat mitigated in the past few decades by the use of unleaded gasoline (10), but industrial inputs and the agronomic application of fertilizers, pesticides, and metal-contaminated sewage continue to contribute to metal accumulation in the soil (20). The immediate toxicity of soil metals to soil organisms is moderated by metal immobilization by soil colloidal components. However, metal ions may be mobilized by changes in physical and chemical conditions of the soil environment, including pH decrease, change in redox potential, and enhanced decomposition of organic matter, posing a considerable challenge to heavy metal-sensitive soil biota (19,21).Arbuscular mycorrhizal (AM) fungi (Glomeromycota) are one of the most prominent soil microorganisms (37). They expand the interface between plants and the soil environment and contribute to plant uptake of macronutrients P (29) and N (1) as well as micronutrients Cu (29) and Zn (8). AM fungi are also involved in plant interactions with soil toxic metals, either by alleviating metal toxicity to the host or by accentuating it (for reviews, see references 9, 28, 3...

Arbuscular mycorrhiza of Deschampsia cespitosa (Poaceae) at different soil depths in highly metal-contaminated site in southern Poland

“…However, taking into account very low concentrations of bioavailable forms of Pb (max. 7 mg kg A toxic effect of Cd, Zn and Pb on mycorrhizal fungi as well as their resistance to these metals was also reported by other authors [26,[52][53][54][55]. In the present field experiment with spontaneous vegetation mycorrhizal colonization was high in soil layers with the concentration of bioavailable Cd lower than 20 mg kg −1 (Fig.…”

Aspects of mycorrhizal colonization in adaptation of sweet marjoram (Origanum majorana L.) grown on industrially polluted soil

“…According to Azcon et al (2010), AMF symbiosis may contribute to phytoremediation via strategies such as HM sequestration or accumulation, keeping metal concentrations in the plants below critical values and improving plant growth and nutrition. The specific role of AMF in the host exposure to metal stress and in the progression of the host stress response depends on a variety of factors, including plant species and ecotype, fungal species and ecotype, and metal availability (Pawlowska et al, 2004).…”

Heavy metals and woody plants - biotechnologies for phytoremediation

“…Arbuscular mychorrhizas are also well known to be involved in the metal uptake; their presence in the soil may significantly affect the plant response to metal stress (Pawloska & Charvat 2004). A vast amount of literature is available on the effects of my corrhizal colonisation of plants living in heavy metal-polluted soils (Göhre & Pas zkowski 2006), on the protective role of my corrhizas against heavy-metal induced oxi dative stress (Schützendübel & Polle 2002), and on their possible role in remediation (Khan et al 2000, Audet & Charest 2007b.…”