Nickel-tolerant ectomycorrhizal Pisolithus albus ultramafic ecotype isolated from nickel mines in New Caledonia strongly enhance growth of the host plant Eucalyptus globulus at toxic nickel concentrations

Ectomycorrhizal (ECM) Pisolithus albus (Cooke & Massee), belonging to the ultramafic ecotype isolated in nickel-rich serpentine soils from New Caledonia (a tropical hotspot of biodiversity) and showing in vitro adaptive nickel tolerance, were inoculated to Eucalyptus globulus Labill used as a Myrtaceae plant-host model to study ectomycorrhizal symbiosis. Plants were then exposed to a nickel (Ni) dose–response experiment with increased Ni treatments up to 60 mg kg − 1 soil as extractable Ni content in serpentine soils. Results showed that plants inoculated with ultramafic ECM P. albus were able to tolerate high and toxic concentrations of Ni (up to 60 μg g − 1) while uninoculated controls were not. At the highest Ni concentration tested, root growth was more than 20-fold higher and shoot growth more than 30-fold higher in ECM plants compared with control plants. The improved growth in ECM plants was associated with a 2.4-fold reduction in root Ni concentration but a massive 60-fold reduction in transfer of Ni from root to shoots. In vitro, P. albus strains could withstand high Ni concentrations but accumulated very little Ni in its tissue. The lower Ni uptake by mycorrhizal plants could not be explained by increased release of metal-complexing chelates since these were 5- to 12-fold lower in mycorrhizal plants at high Ni concentrations. It is proposed that the fungal sheath covering the plant roots acts as an effective barrier to limit transfer of Ni from soil into the root tissue. The degree of tolerance conferred by the ultramafic P. albus isolates to growth of the host tree species is considerably greater than previously reported for other ECM. The primary mechanisms underlying this improved growth were identified as reduced Ni uptake into the roots and markedly reduced transfer from root to shoot in mycorrhizal plants. The fact that these positive responses were observed at Ni concentrations commonly observed in serpentinic soils suggests that ultramafic ecotypes of P. albus could play an important role in the adaptation of tree species to soils containing high concentrations of heavy metals and aid in strategies for ecological restoration.

Philippe Jourand, Marc Ducousso, Robert Reid, Clarisse Majorel, Clément Richert, Jennifer Riss and Michel Lebrun