Tracking nickel‐adaptive biomarkers in Pisolithus albus from New Caledonia using a transcriptomic approach

Abstract

The fungus Pisolithus albus forms ectomycorrhizal (ECM) associations with plants growing on extreme ultramafic soils, which are naturally rich in heavy metals such as nickel. Both nickel-tolerant and nickel-sensitive isolates of P. albus are found in ultramafic soils in New Caledonia, a biodiversity hotspot in the Southwest Pacific. The aim of this work was to monitor the expression of genes involved in the specific molecular response to nickel in a nickel-tolerant P. albus isolate. We used pyrosequencing and quantitative polymerase chain reaction (qPCR) approaches to investigate and compare the transcriptomes of the nickel-tolerant isolate MD06-337 in the presence and absence of nickel. A total of 1,071,375 sequencing reads were assembled to infer expression patterns of 19,518 putative genes. Comparison of expression levels revealed that 30% of the identified genes were modulated by nickel treatment. The genes, for which expression was induced most markedly by nickel, encoded products that were putatively involved in a variety of biological functions, such as the modification of cellular components (53%), regulation of biological processes (27%) and molecular functions (20%). The 10 genes that pyrosequencing analysis indicated were induced the most by nickel were characterized further by qPCR analysis of both nickel-tolerant and nickel-sensitive P. albus isolates. Five of these genes were expressed exclusively in nickel-tolerant isolates as well as in ECM samples in situ, which identified them as potential biomarkers for nickel tolerance in this species. These results clearly suggest a positive transcriptomic response of the fungus to nickel-rich environments. The presence of both nickel-tolerant and nickel-sensitive fungal phenotypes in ultramafic soils might reflect environment-dependent phenotypic responses to variations in the effective concentrations of nickel in heterogeneous ultramafic habitats.

Environmental and Geographical Factors Structure Soil Microbial Diversity in New Caledonian Ultramafic Substrates: A Metagenomic Approach

“…In New Caledonia, studies have demonstrated that the presence of AMF improves plant tolerance to nickel [102,103] and also the existence of nickel-tolerant ECM fungal Pisolithus albus isolates [36]. Furthermore, in these types of soils, certain bacterial strains known to be nickel-resistant and nickel-hyperaccumulators are present [99,100].…”

“…Based on the geographic discontinuity of ultramafic massifs and the existence of different plant formations, habitats on ultramafic outcrops are consequently heterogeneous and could potentially harbour distinct microbial communities. Studies performed in New Caledonia on these types of soils have focused on bacterial and fungal adaptation to nickel [35,36], the effects of mining activities and the restoration of microbial community structure [37], the mycorrhizal status of different plants growing on these substrates [38,39], or again the effects of arbuscular mycorrhizal fungi (AMF) on plant adaptations to nickel-rich substrates [40,41]. However, none of these studies have focused on soil microbial composition on ultramafic substrates in different plant formations and at different sites along New Caledonia.…”

Mycorrhizal ecology on serpentine soils

“…Isolates of Suillus (Basidiomycota) from mineral-polluted soils showed greater tolerance to Zn and Cd, but not to copper (Cu) or Ni, and the Zn-tolerant strains were obtained from a Zncontaminated site (Colpaert et al 2000;Meharg and Cairney 2000;Adriaensen et al 2004). Similarly Nitolerant and Ni-sensitive strains of Pisolithus albus (Basidiomycota) have been isolated in New Caledonia (Jourand et al 2010;Majorel et al 2012). In Oidiodendron (Ascomycota), an ericoid mycorrhizal fungus, isolates from serpentine soils showed genetic polymorphism in a functional gene that differed from other isolates obtained at sites with mineral pollution (Vallino et al 2011).…”

Ectomycorrhizae and tree seedling nitrogen nutrition in forest restoration

“…Not all fungal isolates from a contaminated site will be tolerant to the metals found on that site (Majorel et al 2012). A standard technique for screening tolerant isolates is to grow them in pure culture in liquid or solidified nutrient media amended with a range of concentrations of toxic metals.…”