Firing Range Soils Yield a Diverse Array of Fungal Isolates Capable of Organic Acid Production and Pb Mineral Solubilization

Abstract

e Anthropogenic sources of lead contamination in soils include mining and smelting activities, effluents and wastes, agricultural pesticides, domestic garbage dumps, and shooting ranges. While Pb is typically considered relatively insoluble in the soil environment, some fungi may potentially contribute to mobilization of heavy metal cations by means of secretion of low-molecularweight organic acids (LMWOAs). We sought to better understand the potential for metal mobilization within an indigenous fungal community at an abandoned shooting range in Oak Ridge, TN, where soil Pb contamination levels ranged from 24 to >2,700 mg Pb kg dry soil ؊1 . We utilized culture-based assays to determine organic acid secretion and Pb-carbonate dissolution of a diverse collection of soil fungal isolates derived from the site and verified isolate distribution patterns within the community by 28S rRNA gene analysis of whole soils. The fungal isolates examined included both ascomycetes and basidiomycetes that excreted high levels (up to 27 mM) of a mixture of LMWOAs, including oxalic and citric acids, and several isolates demonstrated a marked ability to dissolve Pb-carbonate at high concentrations up to 10.5 g liter ؊1 (18.5 mM) in laboratory assays. Fungi within the indigenous community of these highly Pb-contaminated soils are capable of LMWOA secretion at levels greater than those of well-studied model organisms, such as Aspergillus niger. Additionally, these organisms were found in high relative abundance (>1%) in some of the most heavily contaminated soils. Our data highlight the need to understand more about autochthonous fungal communities at Pb-contaminated sites and how they may impact Pb biogeochemistry, solubility, and bioavailability, thus consequently potentially impacting human and ecosystem health.

Oxalic acid: a signal molecule for fungus‐feeding bacteria of the genus Collimonas?

“…In the process of wood decomposition by brown or white rot fungi, oxalic acid is released and acts as mediator in the degradation of lignin (Shimada et al, 1997;Hastrup et al, 2012). Plant-associated, ecto-mycorrhizal fungi, but also saprotrophic soil fungi (Sullivan et al, 2012) secrete citric-and oxalic acid to release inorganic nutrients and scavenge metals, possibly by chelation and acidification (van Hees et al, 2006;Adeleke et al, 2012). Fast-growing, saprotrophic fungi like Penicillium or Aspergillus are also able to secrete oxalic acid in order to mineralize inorganic phosphorus (Dutton and Evans, 1996).…”

“…Despite the formation of oxalate complexes on the long term, free oxalic acid is also present in soils near zones (roots, hyphae) of active oxalic acid exudation (Jaitz et al, 2011). Among fungal exudates, oxalic acid is the major one, being exuded in concentrations up to 20 mM (Guggiari et al, 2011;Sullivan et al, 2012). Some bacterial groups have specialized to use oxalic acid and oxalate complexes as a carbon source.…”

Pyromorphite formation in a fungal biofilm community growing on lead metal

“…Such toxicity resulted in the widespread change to Pb-free petrol (gasoline), and the banning of Pbcontaining paints and Pb toys (UNEPCB, DTIE, 2010;WHO, 2011). It has also lead to restrictions in its use for lead weights and jigs in angling, although shooting activities appear unaffected by any such restrictions despite huge amounts of Pb entering the environment through recreational shooting and hunting (Scheuhammer and Norris, 1996;Dermatas et al, 2006;Sullivan et al, 2012). Before the Pb shot ban for wildfowling in the UK, an average of 3 × 10 5 pellets per hectare in the top 15 cm of sediments have been recorded in wetland habitats (Quy, 2010).…”

Transformation of vanadinite [Pb5(VO4)3Cl] by fungi

“…The pH plays a very important role in such mineral transformations by fungi, controlling metal hydrolysis and complexation, mineral dissolution (e.g. silicates, phosphates) and deposition of crystalline material (Barker et al, 1997;Gadd, 1999;2010;Burford et al, 2003a;Debela et al, 2010;Sullivan et al, 2012). The nature and amount of organic acids excreted by fungi are also influenced by the pH, buffering capacity of the medium, and availability of C, P, N and certain trace metals (Gadd, 1999;2010;Sayer and Gadd, 2001;Fomina et al, 2004;2007;Gadd and Fomina, 2011;Sullivan et al, 2012).…”