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

• Published in: Molecular ecology 2012-05, Vol.21 (9), p.2208-2223
• Main Authors: MAJOREL, CLARISSE, HANNIBAL, LAURE, SOUPE, MARIE-ESTELLE, CARRICONDE, FABIAN, DUCOUSSO, MARC, LEBRUN, MICHEL, JOURAND, PHILIPPE
• Format: Article
• Language: English
• Subjects: Adaptation, Physiological - genetics; Basidiomycota - drug effects; Basidiomycota - genetics; Basidiomycota - isolation & purification; Basidiomycota - metabolism; Biodiversity; Biomarkers; Ecosystem; ectomycorrhiza; Gene Expression Regulation, Fungal; Genetic Variation; Molecular Sequence Annotation; Mycorrhizae - drug effects; Mycorrhizae - genetics; Mycorrhizae - isolation & purification; Mycorrhizae - metabolism; New Caledonia; Nickel; Nickel - metabolism; Nickel - pharmacology; Phylogeny; Pisolithus; Pisolithus albus; Plant growth; Plants - microbiology; pyrosequencing; Sequence Analysis, DNA; Soil Microbiology; Soils; Transcriptome
• ISSN: 0962-1083; 1365-294X
• DOI: 10.1111/j.1365-294X.2012.05527.x

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.