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Evidence of adaptive tolerance to nickel in isolates of Cenococcum geophilum from serpentine soils

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Abstract

Selection for metal-tolerant ecotypes of ectomycorrhizal (ECM) fungi has been reported in instances of metal contamination of soils as a result of human activities. However, no study has yet provided evidence that natural metalliferous soils, such as serpentine soils, can drive the evolution of metal tolerance in ECM fungi. We examined in vitro Ni tolerance in isolates of Cenococcum geophilum from serpentine and non-serpentine soils to assess whether isolates from serpentine soils exhibited patterns consistent with adaptation to elevated levels of Ni, a typical feature of serpentine. A second objective was to investigate the relationship between Ni tolerance and specific growth rates (µ) among isolates to increase our understanding of possible tolerance/growth trade-offs. Isolates from both soil types were screened for Ni tolerance by measuring biomass production in liquid media with increasing Ni concentrations, so that the effective concentration of Ni inhibiting fungal growth by 50% (EC50) could be determined. Isolates of C. geophilum from serpentine soils exhibited significantly higher tolerance to Ni than non-serpentine isolates. The mean Ni EC50 value for serpentine isolates (23.4 µg ml−1) was approximately seven times higher than the estimated value for non-serpentine isolates (3.38 µg ml−1). Although there was still a considerable variation in Ni sensitivity among the isolates, none of the serpentine isolates had EC50 values for Ni within the range found for non-serpentine isolates. We found a negative correlation between EC50 and µ values among isolates (r = −0.555). This trend, albeit only marginally significant (P = 0.06), indicates a potential trade-off between tolerance and growth, in agreement with selection against Ni tolerance in “normal” habitats. Overall, these results suggest that Ni tolerance arose among serpentine isolates of C. geophilum as an adaptive response to Ni exposure in serpentine soils.

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Acknowledgments

This study was part of S.C. Gonçalves PhD project funded by FCT (PRAXIS XXI/BD/16257/98). We are grateful to Greg Douhan and Dan Panaccione for providing us the isolates of C. geophilum from California and Maryland, USA, respectively. Thanks are due to S.R. Costa, M.T. Gonçalves, C. Moura, and A. Portugal for their critical reading of the manuscript.

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Authors and Affiliations

  1. Centro de Ecologia Funcional, Departamento de Botânica, Faculdade de Ciências e Tecnologia, Universidade de Coimbra, 3000-456, Coimbra, Portugal

    Susana C. Gonçalves & Helena Freitas

  2. Faculdade de Ciências, Centro de Biologia Ambiental, Departamento de Biologia Vegetal, Universidade de Lisboa, 1749-016, Lisboa, Portugal

    M. Amélia Martins-Loução

  3. Museu Nacional de História Natural, Universidade de Lisboa, Jardim Botânico, 1250-102, Lisboa, Portugal

    M. Amélia Martins-Loução

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  1. Susana C. Gonçalves
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  2. M. Amélia Martins-Loução
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  3. Helena Freitas
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Correspondence to Susana C. Gonçalves.

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Gonçalves, S.C., Martins-Loução, M.A. & Freitas, H. Evidence of adaptive tolerance to nickel in isolates of Cenococcum geophilum from serpentine soils. Mycorrhiza 19, 221–230 (2009). https://doi.org/10.1007/s00572-008-0211-4

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