Organic Acids Induce Tolerance to Zinc- and Copper-Exposed Fungi Under Various Growth Conditions

Abstract

Heavy metals, Zn and Cu, in high concentration (2 mM for Zn and 0.5 mM for Cu) have some inhibiting effect on the growth of Aspergillus niger and Penicillium citrinum. Toxic effects of these metals considerably depend on cultivation conditions including nitrogen sources, pH of nutrient media, and its consistency (presence or absence of agar). In general, nitrate media provides less inhibiting effect on fungal growth under heavy metal exposure than ammonium-containing media. Adding of Zn in nitrate media induces oxalic acid production by fungi. Importance of oxalic acid production in detoxification of heavy metals is confirmed by the formation of Zn-containing crystals in fungal cultures. Cu bringing to the cultural media had no stimulating effect on oxalic acid production as well as no copper-containing crystals were observed. But proceeding from essential increase in oxalic acid production during a long-term fungi adaptation to Cu, it may be proposed that oxalic acid plays some functional role in Cu tolerance of fungi as well. It may be concluded that the role of organic acids and oxalate, in particular, in fungi tolerance and adaptation to heavy metals can be determined by the nature of the metal and its ability to form stable complexes with an acid anion. Stimulating effect of metals on acid production is not universal for all species of fungi and largely depends on metal concentration, nitrogen form in a medium, and other cultivation conditions.

The role of organic acids in heavy metal tolerance in plants

“…On the other hand, when maize plants were exposed to 100 µm Cu or Cd in a hydroponic culture, significant secretion of citrate was not observed, in contrast to that observed in the presence of Al (Chaffai, Tekitek, and El Ferjani, 2006). It should be noted that the extracellular production of organic acids is considered an important mechanism in increasing heavy metal tolerance not only in higher terrestrial plants, but also in fungi (Sazanova et al, 2015) and in hydrophytes (Kurilenko and Osmolovskaya, 2015).…”

Entomopathogenic fungi-based mechanisms for improved Fe nutrition in sorghum plants grown on calcareous substrates

“…Fungi (EPF included) are known to alter their environment by releasing organic acids [ 67 ], and the concentrations of nutrients such as Fe, Cu, and Ag [ 68 ], Zn [ 69 ] or P [ 70 ] increase as a result. The released organic acids lower the pH of the medium and increase the solubility of Fe oxides.…”

NmeA, a novel efflux transporter specific for nucleobases and nucleosides, contributes to metal resistance in Aspergillus nidulans

“…This possibility has been supported previously in fungi and plants. More specifically, the toxic effect of Zn and Cu on Aspergillus niger and Penicillium citrinum growth has been reported to depend on physiological conditions related to nitrogen sources, and in particular, nitrate media provided reduced metal toxicity compared to ammonium‐containing media (Sazanova et al ., ). These findings are compatible with the idea that ammonium represses purine catabolism and leads to depletion of purine metabolites, which in turn leads to reduced metal resistance.…”

“…Other studies have further shown that various abiotic stresses activate allantoin and allantoate accumulation, conferring increased stress resistance to plants (Yesbergenova et al ., , Alamillo et al ., , Watanabe et al ., , Irani and Todd, ). Finally, there are also reports that show that certain nucleobases (Rodgers and Armentrout, ; Brandi‐Blanco et al ., ) and other metabolites, such as oxalic acid (Sazanova et al ., ) or proline (Dinakar et al ., ) chelate metals. In one case, metal chelation has been further shown to contribute to metal tolerance in fungi (Sazanova et al ., ).…”