Ectomycorrhizal fungal diversity associated with endemic Tristaniopsis spp. (Myrtaceae) in ultramafic and volcano-sedimentary soils in New Caledonia

Abstract

New Caledonian serpentine (ultramafic) soils contain high levels of toxic heavy metals, in particular nickel, (up to 20 g kg−1) and are deficient in essential elements like carbon, nitrogen and phosphorus while having a high magnesium/calcium ratio. Although previous studies showed that ectomycorrhizal symbioses could play an important role in the adaptation of the endemic plants to ultramafic soils (FEMS Microbiol Ecol 72:238–49, 2010), none of them have compared the diversity of microbial communities from ultramafic vs non-ultramafic soils in New Caledonia. We explored the impact of edaphic characteristics on the diversity of ectomycorrhizal (ECM) fungi associated with different endemic species of Tristaniopsis (Myrtaceae) growing under contrasting soil conditions in the natural ecosystems of New Caledonia. ECM root tips were thus sampled from two different ultramafic sites (Koniambo massif and Desmazures forest) vs two volcano-sedimentary ones (Arama and Mont Ninndo). The molecular characterization of the ECM fungi through partial sequencing of the ITS rRNA gene revealed the presence of different dominant fungal genera including, both soil types combined, Cortinarius (36.1%), Pisolithus (18.5%), Russula (13.4%), Heliotales (8.2%) and Boletellus (7.2%). A high diversity of ECM taxa associated with Tristaniopsis species was found in both ultramafic and volcano-sedimentary soils but no significant differences in ECM genera distribution were observed between both soil types. No link could be established between the phylogenetic clustering of ECM taxa and their soil type origin, thus suggesting a possible functional—rather than taxonomical—adaptation of ECM fungal communities to ultramafic soils.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

  2. Amir H, Perrier N, Rigault F, Jaffré T (2007) Relationships between Ni-hyperaccumulation and mycorrhizal status of different endemic plant species from New Caledonian ultramafic soils. Plant Soil 293:23–35

    CAS  Article  Google Scholar 

  3. Bordez L, Jourand P, Ducousso M, Carriconde F, Cavaloc Y, Santini S, Claverie JM, Wantiez L, Leveau A, Amir H (2016) Distribution patterns of microbial communities in ultramafic landscape: a metagenetic approach highlights the strong relationships between diversity and environmental traits. Mol Ecol 25:2258–2272

    CAS  Article  PubMed  Google Scholar 

  4. Branco S (2010) Serpentine soils promote ectomycorrhizal fungal diversity. Mol Ecol 19:5566–5576

    Article  PubMed  Google Scholar 

  5. Branco S, Ree RH (2010) Serpentine soils do not limit mycorrhizal fungal diversity. PLoS One 5:e11757-7

  6. Brooks RR (1987) Serpentine and its vegetation: a multidisciplinary approach. Croom Helm, London and Sydney

    Google Scholar 

  7. Cavander-Bares J, Ackerly D, Baum D, Bazzaz F (2004) Phylogenetic over dispersion in Floridian oak communities. Am Nat 163:823–843

    Article  Google Scholar 

  8. Chaintreuil C, Rigault F, Moulin L, Jaffre T, Fardoux J, Giraud E, Dreyfus B, Bailly X (2007) Nickel resistance determinants in Bradyrhizobium strains from nodules of the endemic New Caledonia legume Serianthes calycina. Appl Environ Microbiol 73:8018–8022

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Colwell RK (2009) EstimateS: statistical estimation of species richness and shared species from samples. Version 8.2. User’s Guide and application published at: http://purl.oclc.org/estimates.

  10. Colwell RK, Mao CX, Chang J (2004) Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85:2717–2727

    Article  Google Scholar 

  11. Daghino S, Murat C, Sizzano E, Girlanda M, Perotto S (2012) Fungal diversity is not determined by mineral and chemical differences in serpentine substrates. PLoS One 7:e44233-13

  12. Diedhiou AG, Selosse MA, Galiana A, Diabate M, Dreyfus B, Ba AM, de Faria SM, Bena G (2010) Multi-host ectomycorrhizal fungi are predominant in a Guinean tropical rainforest and shared between canopy trees and seedlings. Environ Microbiol 12:2219–2232

    CAS  PubMed  Google Scholar 

  13. Fitzsimons M, Miller R (2010) Serpentine soil has little influence on the root-associated microbial community composition of the serpentine tolerant grass species Avenula sulcata. Plant Soil 330:393–405

    CAS  Article  Google Scholar 

  14. Fritsch E (2012) Les sols. In: Bonvallot J, Gay JC, Habert E (eds) Atlas de la Nouvelle-Calédonie. Congrès de la Nouvelle-Calédonie, Marseille (FRA); Nouméa: IRD, pp 73–76

    Google Scholar 

  15. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    CAS  Article  PubMed  Google Scholar 

  16. Gehring CA, Theimer TC, Whitham TG, Keim P (1998) Ectomycorrhizal fungal community structure of pinyon pines growing in two environmental extremes. Ecology 79:1562–1572

    Article  Google Scholar 

  17. Gillespie TW, Jaffré T (2003) Tropical dry forests in New Caledonia. Biodivers Conserv 12:1687–1697

    Article  Google Scholar 

  18. Héry M, Philippot L, Mériaux E, Poly F, le Roux X, Nazaret S, Jaffré T, Normand P, Navarro E (2003) Adaptation to nickel spiking of bacterial communities in neocaledonian soils. Environ Microbiol 5:3–12

    Article  PubMed  Google Scholar 

  19. Jaffré T, Bouchet P, Veillon JM, Mackee HS (1987) Changements dans la végétation de la Nouvelle-Calédonie au cours du Tertiaire: la végétation et la flore des roches ultrabasiques, vol 4. Bulletin du Museum. National d’Histoire Naturelle, Paris

    Google Scholar 

  20. Joner EJ, Leyval C, Colpaert JV (2006) Ectomycorrhizas impede phytoremediation of polycyclic aromatic hydrocarbons (PAHs) both within and beyond the rhizosphere. Environ Pollut 142:34–38

    CAS  Article  PubMed  Google Scholar 

  21. Jourand P, Ducousso M, Loulergue-Majorel C, Hannibal L, Santoni S, Prin Y et al (2010a) Ultramafic soils from New Caledonia structure Pisolithus albus in ecotype. FEMS Microbiol Ecol 72:238–249

    CAS  Article  PubMed  Google Scholar 

  22. Jourand P, Ducousso M, Reid R, Majorel C, Richert C, Riss J, Lebrun M (2010b) 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. Tree Physiol 30:1311–1319

    CAS  Article  PubMed  Google Scholar 

  23. Krznaric E, Verbruggen N, Wevers JHL, Carleer R, Vangronsveld J, Colpaert JV (2009) Cd-tolerant Suillus luteus: a fungal insurance for pines exposed to Cd. Environ Pollut 157:1581–1588

    CAS  Article  PubMed  Google Scholar 

  24. L’Huillier L, Jaffré T, Wulff A (2010) Mines et environnement en Nouvelle-Calédonie: les milieux sur substrats ultramafiques et leur restauration. Edition IAC, Noumea, Nouvelle Calédonie

    Google Scholar 

  25. Leyval C, Turnau K, Haselwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7:139–153

    CAS  Article  Google Scholar 

  26. Morat P, Jaffré T, Tronchet F, Munzinger J, Pillon Y, Veillon JM, Chalopin M, Birnbaum P, Rigault F, Dagostini G, Tinel J, Lowry PP (2012) The taxonomic reference base Florical and characteristics of the native vascular flora of New Caledonia. Adansonia 34:179–221

    Article  Google Scholar 

  27. Moser A, Frank J, D’Allura J, Southworth D (2009) Ectomycorrhizal communities of Quercus garryana are similar on serpentine and nonserpentine soils. Plant Soil 315:185–194

    CAS  Article  Google Scholar 

  28. Moyersoen B, Beever RE, Martin F (2003) Genetic diversity of Pisolithus in New Zealand indicates multiple long-distance dispersal from Australia. New Phytol 160:569–579

    Article  Google Scholar 

  29. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    CAS  Article  PubMed  Google Scholar 

  30. Navarro E, Jaffré T, Gauthier D, Gourbiere F, Rinaudo G, Simonet P, Normand P (1999) Distribution of Gymnostoma spp. microsymbiotic Frankia strains in New Caledonia is related to soil type and to host-plant species. Mol Ecol 8:1781–1788

    CAS  Article  PubMed  Google Scholar 

  31. Nicholas K, Nicholas H, Deerfield D (1997) GeneDoc:analysis and visualization of genetic variation. Embnew News 4:14

  32. Perrier N, Amir H, Colin F (2006) Occurrence of mycorrhizal symbioses in the metal-rich lateritic soils of the Koniambo Massif, New Caledonia. Mycorrhiza 16:449–458

    Article  PubMed  Google Scholar 

  33. Rothschild LJ, Mancinelli RL (2001) Life in extreme environments. Nature 409:1092–1101

    CAS  Article  PubMed  Google Scholar 

  34. Schechter SP, Bruns TD (2008) Serpentine and non-serpentine ecotypes of Collinsia sparsiflora associate with distinct arbuscular mycorrhizal fungal assemblages. Mol Ecol 17:3198–3210

    CAS  Article  PubMed  Google Scholar 

  35. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, Amsterdam; Boston

    Google Scholar 

  36. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. Urban A, Puschenreiter M, Strauss J, Gorfer M (2008) Diversity and structure of ectomycorrhizal and co-associated fungal communities in a serpentine soil. Mycorrhiza 18:339–354

    Article  PubMed  Google Scholar 

  39. White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gefland DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, London, pp 315–322

    Google Scholar 

Download references

Acknowledgements

The Agence Nationale de la Recherche, ANR 07 BIODIV ULTRABIO, financially supported this research work. We are also thankful to the Higher Education Commission of Pakistan for supporting this work through a PhD fellowship.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Antoine Galiana.

Electronic supplementary material

Supplemental Figure S1

General geographical map describing the New Caledonian archipelago, location of sites on ultramafic (in grey) and volcano sedimentary (in white) soils where Tristaniopsis spp. ECM root tips were collected. Ultramafic sites: (1) Forêt Desmazures and (2) Koniambo massif; volcano-sedimentary sites: (3) Col d’Arama and (4) Mount Ninndo (PDF 262 kb)

Supplemental Figure S2

Species accumulation curves obtained for ECM a) in ultramafic soils; and b) in volcano-sedimentary soils (DOCX 78 kb)

Supplemental Table S1

Names, geographic coordinates, altitudes of the sampling sites and identification of the Tristaniopsis species present on each site (DOCX 76 kb)

Supplemental Table S2

List of ECM fungal taxa found in this study indicating their genus affiliation, Genbank accession number and closest BLAST hit (DOCX 42 kb)

Supplemental Table S3

Number of root tips successfully sequenced in each ECM genus obtained from the different study sites and Tristaniopsis species (DOCX 60 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Waseem, M., Ducousso, M., Prin, Y. et al. Ectomycorrhizal fungal diversity associated with endemic Tristaniopsis spp. (Myrtaceae) in ultramafic and volcano-sedimentary soils in New Caledonia. Mycorrhiza 27, 407–413 (2017). https://doi.org/10.1007/s00572-017-0761-4

Download citation

Keywords

  • Serpentine soils
  • Cortinarius
  • Pisolithus
  • Russula
  • Nickel tolerance
  • Fungal diversity