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Structure and phylogenetic diversity of post-fire ectomycorrhizal communities of maritime pine

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Abstract

Environmental disturbances define the diversity and assemblage of species, affecting the functioning of ecosystems. Fire is a major disturbance of Mediterranean pine forests. Pines are highly dependent on the ectomycorrhizal (EM) fungal symbiosis, which is critical for tree recruitment under primary succession. To determine the effects of time since fire on the structure and recovery of EM fungal communities, we surveyed the young Pinus pinaster regenerate in three sites differing in the elapsed time after the last fire event. Pine roots were collected, and EM fungi characterized by sequencing the internal transcribed spacer (ITS) and the large subunit (LSU) regions of the nuclear ribosomal (nr)-DNA. The effects of the elapsed time after fire on the EM community structure (richness, presence/absence of fungi, phylogenetic diversity) and on soil properties were analysed.

Fungal richness decreased with the elapsed time since the fire; although, the phylogenetic diversity of the EM community increased. Soil properties were different depending on the elapsed time after fire and particularly, the organic matter, carbon-to-nitrogen (C/N) ratio, nitrogen and iron significantly correlated with the assemblage of fungal species. Ascomycetes, particularly Tuberaceae and Pezizales, were significantly over-represented on saplings in the burned site. On seedlings, a significant over-representation of Rhizopogonaceae and Atheliaceae was observed in the most recently burned site, while other fungi (i.e. Cortinariaceae) were significantly under-represented. Our results are consistent with the hypothesis that fire can act as a selective agent by printing a phylogenetic signal on the EM fungal communities associated with naturally regenerated pines, pointing out to some groups as potential fire-adapted fungi.

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References

  • Agerer R (1987–1998) Colour atlas of ectomycorrhizae. Einhirn-Verlag Eduard Dietenberger, Munich

  • Agerer R (2001) Exploration types of ectomycorrhizae. A proposal to classify extomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114

    Article  Google Scholar 

  • Anderson TM, Lachance M-A, Starmer WT (2004) The relationship of phylogeny to community structure: the cactus yeast community. Am Nat 164:709–721

    Article  Google Scholar 

  • Avis PG, McLaughlin DJ, Dentinger BC, Reich PB (2003) Long-term increase in nitrogen supply alters above and below-ground ectomycorrhizal communities and increases the dominance of Russula spp. in a temperate oak savannah. New Phytol 160:239–253

    Article  Google Scholar 

  • Baar J, Horton TR, Kretzer AM, Bruns TD (1999) Mycorrhizal colonization of Pinus muricata from resistant propagules after a stand-replacing wildfire. New Phytol 143:409–418

    Article  Google Scholar 

  • Bastias BA, Xu Z, Cairney JWG (2006) Influence of long-term repeated prescribed burning on mycelial communities of ectomycorrhizal fungi. New Phytol 172:149–158

    Article  CAS  PubMed  Google Scholar 

  • Berbee ML, Taylor JW (1993) Dating the evolutionary radiations of the true fungi. Can J Bot 71:1114–1127

    Article  Google Scholar 

  • Branco S, Ree RH (2010) Serpentine soils do not limit mycorrhizal fungal diversity. PlosOne 5:1–7

    Article  Google Scholar 

  • Bruns T, Biartondo MI, Taylor L (2002) Host specificity in ectomycorrhizal communities: what do the exceptions tell us. Integr Comp Biol 42:352–359

    Article  PubMed  Google Scholar 

  • Buscardo E, Rodríguez-Echeverría S, Martin MP, de Angelis P, Pereira JS, Freitas H (2010) Impact of wildfire return interval on the ectomycorrhizal resistant propagules communities of a Mediterranean open forest. Fungal Biol 114:628–636

    Article  PubMed  Google Scholar 

  • Buscardo E, Freitas H, Pereira JS, de Angelis P (2011) Common environmental factors explain both ectomycorrhizal species diversity and pine regeneration variability in a post-fire Mediterranean forest. Mycorrhiza 21:549–558

    Article  PubMed  Google Scholar 

  • Cairney JWG, Bastias BA (2007) Influences of fire on forest soil fungal communities. Can J For Res 37:207–215

    Article  Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  • Certini G (2005) Effects of fire on properties of forest soils: a review. Oecologia 143:1–10

    Article  PubMed  Google Scholar 

  • Claridge AW, Trappe JM, Mills DJ, Claridge DL (2009) Diversity and habitat relationships of hypogeous fungi. III. Factors influencing the occurrence of fire-adapted species. Mycol Res 113:792–801

    Article  PubMed  Google Scholar 

  • Dahlberg A, Schimmel J, Taylor AFS, Johannesson H (2001) Post-fire legacy of ectomycorrhizal fungal communities in the Swedish boreal forest in relation to fire severity and logging intensity. Biol Conserv 100:151–161

    Article  Google Scholar 

  • Dickie IA, Dentinger BTM, Avis PG, McLaughlin DJ, Reich PB (2009) Ectomycorrhizal communities of oak savana are distinct from forest communities. Mycologia 101:473–483

    Article  CAS  PubMed  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed Central  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Grogan P, Baar J, Bruns TD (2000) Below-ground ectomycorrhizal community structure in a recently burned bishop pine forest. J Ecol 88:1051–1062

    Article  Google Scholar 

  • Hart SC, DeLuca TH, Newman GS, MacKenzie MD, Boyle SI (2005) Post-fire vegetative dynamics as drivers of microbial community structure and function in forest soils. For Ecol Manag 220:166–184

    Article  Google Scholar 

  • Hibbet DS (2006) A phylogenetic overview of the Agaricomycotina. Mycologia 96:917–925

    Article  Google Scholar 

  • Horner-Devine MC, Bohannan BJM (2006) Phylogenetic clustering and overdispersion in bacterial communities. Ecology S100-S108

  • Horton TR, Cazares E, Bruns TD (1998) Ectomycorrhizal, vesicular-arbuscular and dark septate fungal colonization of bishop pine (Pinus muricata) seedlings in the first 5 months of growth after wildfire. Mycorrhiza 8:11–18

    Article  Google Scholar 

  • James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J et al (2006) Reconstruction the early evolution of fungi using a six gene phylogeny. Nature 443:818–822

    Article  CAS  PubMed  Google Scholar 

  • Jonsson L, Dahlberg A, Nilsson MC, Zackrisson O, Karen O (1999) Ectomycorrhizal fungal communities in late-successional Swedish boreal forests, and their composition following wildfire. Mol Ecol 8:205–215

    Article  Google Scholar 

  • Johnson D, Martin F, Cairney JWG, Anderson IC (2012) The importance of individuals: intraspecific diversity on mycorrhizal plants and fungi in ecosystems. New Phytol 194:614–628

    Article  PubMed  Google Scholar 

  • Keeley JE, Bond WJ, Bradstock RA, Pausas JG, Rundel PW (2012) Fire in Mediterranean Ecosystems. Ecology, Evolution and Management. Cambridge University Press, NY

    Google Scholar 

  • Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464

    Article  CAS  PubMed  Google Scholar 

  • Kennedy PG, Peay KG, Bruns TD (2009) Root tip competition among ectomycorrhizal fungi: are priority effects a rule or an exception? Ecology 90:2098–2107

    Article  PubMed  Google Scholar 

  • Kennedy P (2010) Ectomycorrhizal fungi and interspecific competition: species interactions, community structure, coexistence mechanisms and future research directions. New Phytol 187:895–910

    Article  PubMed  Google Scholar 

  • Kipfer T, Moser B, Egli S, Wohlgemuth T, Ghazoul J (2011) Ectomycorrhizal succession patterns in Pinus sylvestris forests after stand-replacing fire in the Central Alps. Oecologia 167:219–228

    Article  PubMed  Google Scholar 

  • LeDuc SD, Lilleskov EA, Horton TR, Rothstein DE (2012) Ectomycorrhizal fungal succession coincides with shifts in organic nitrogen availability and canopy closure in post-wildfire jack pine forests. Oecologia. doi:10.1007/s00442-012-2471-0

    PubMed  Google Scholar 

  • Legendre P, De Cáceres M, Bocard D (2010) Community surveys through space and time: testing the space-time interaction in the absence of replication. Ecology 91:262–272

    Article  PubMed  Google Scholar 

  • Lilleskov EA, Hobbie EA, Fahey TJ (2002) Ectomycorrhizal fungal taxa differing in response to nitrogen deposition also differ in pure culture organic nitrogen use and natural abundance of nitrogen isotopes. New Phytol 154:219–231

    Article  CAS  Google Scholar 

  • Loepfe L, Martinez-Vilalta J, Oliveres J, Piñol J, Lloret F (2010) Feedbacks between fuel reduction and landscape homogenisation determine fire regimes in three Mediterranean areas. For Ecol Manag 259:2366–2374

    Article  Google Scholar 

  • Longo S, Urcelay C, Nouhra E (2011) Long term effects of fire on ectomycorrhizas and soil properties in Nothofagus pumilio foests in Argentina. For Ecol Manag 262:348–354

    Article  Google Scholar 

  • Magurran AE (1988) Ecological diversity and its measurement. Princeton University Press, USA, Princeton

    Book  Google Scholar 

  • Maherali H, Klironomos JN (2007) Influence of Phylogeny on Fungal Community Assembly and Ecosystem Functioning. Science 316:1746–1748

    Article  CAS  PubMed  Google Scholar 

  • McMullan-Fisher SJM, May TW, Robinson RM, Bell TL, Lebel T, Catcheside P, York A (2011) Fungi and fire in Australian ecosystems: a review of current knowledge, management implications and future directions. Aust J Bot 59:70–90

    Article  Google Scholar 

  • Molina R, Trappe JM, Grubisha LC, Spatafora JW (1999) Rhizopogon. In: Cairney JWG, Chambers SM (eds) Ectomycorrhizal fungi key genera in profile. Springer, Berlin, Germany, pp 129–161

    Chapter  Google Scholar 

  • Moncalvo J-M, Nilsson RH, Koster B, Dunham SM, Bernauer T, Matheny PB, McLenon T, Margaritescu S, Wei BM, Garnica S et al (2006) The cantharelloid clade: dealing with incongruent gene trees and phylogenetic reconstruction methods. Mycologia 98:937–948

    Article  PubMed  Google Scholar 

  • Nara K (2009) Spores of ectomycorrhizal fungi: ecological strategies for germination and dormancy. New Phytol 181:245–248

    Article  PubMed  Google Scholar 

  • Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson KH (2008) Intraspecific ITS variability in the Kingdom Fungi as expressed in the international sequence databases and its implications for molecular species identification. Evol Informat 4:193–201

    Google Scholar 

  • Nilsson LO, Wallander H, Gundersen P (2012) Changes in microbial activities and biomasses over a forest floor gradient in C to N ratio. Plant Soil 355:75–86

    Article  CAS  Google Scholar 

  • Oksanen JF, Blanchet G, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2011) Vegan: Community Ecology Package. R package version 2.0-0. http://CRAN.R-project.org/package=vegan

  • Pausas JG, Verdú M (2010) The jungle of methods for evaluating phenotypic and phylogenetic structure of communities. BioScience 60:614–625

    Article  Google Scholar 

  • Peay KG, Kennedy PG, Davies SJ, Tan S, Bruns TD (2010) Potential link between plant and fungal distributions in a dipterocarp rainforest: community and phylogenetic structure of tropical ectomycorrhizal fungi across a plant and soil ecotone. New Phytol 185:529–542

    Article  CAS  PubMed  Google Scholar 

  • Peay KG, Belisle M, Fukami T (2012) Phylogenetic relatedness predicts priority effects in nectar yeast communities. P Roy Soc B 279:749–758

    Article  Google Scholar 

  • Pereira P, Úbeda X, Martin DA (2012) Fire severity effects on ash chemical composition and water extractable elements. Geoderma 191:105–114

    Article  CAS  Google Scholar 

  • R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.rproject.org/

  • Rincón AR, Pueyo JJ (2010) Effect of fire severity and site slope on diversity and structure of the ectomycorrhizal fungal community associated with post-fire regenerated Pinus pinaster Ait. seedlings. For Ecol Manag 260:361–369

    Article  Google Scholar 

  • Rodrigo A, Retana J, Pico FX (2004) Direct regeneration is not the only response of Mediterranean forests to large fires. Ecology 85:716–729

    Article  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal Symbiosis. Academic Press, Cambridge, UK

    Google Scholar 

  • Stendell ER, Horton TR, Bruns TD (1999) Early effects of prescribed fire on the structure of the ectomycorrhizal fungus community in a Sierra Nevada ponderosa pine forest. Mycol Res 103:1353–1359

    Article  Google Scholar 

  • Schoch CL, Sung GH, Pez-Giraldez FL, Townsend JP, Miadlikowska J, Hofstetter V, Robertse B, Matheny PB, Kauff F, Wang Z et al (2009) The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Systematic Biol 58:224–239

    Article  CAS  Google Scholar 

  • Sugiyama J, Hosaka K, Suth SO (2006) Early diverging Ascomycota: phylogenetic divergence and related evolutionary enigmas. Mycologia 98:996–1005

    Article  PubMed  Google Scholar 

  • Tapias R, Climent J, Pardos JA, Gil L (2004) Life history of Mediterranean pines. Plant Ecol 171:53–68

    Article  Google Scholar 

  • Taylor DL, Bruns TD (1999) Community structure of ectomycorrhizal fungi in a Pinus muricata forest: minimal overlap between the mature forest and resistant propagule communities. Mol Ecol 8:1837–1850

    Article  CAS  PubMed  Google Scholar 

  • Tedersoo L, Suvi T, Larsson E, Koljalg U (2006) Diversity and community structure of ectomycorrhizal fungi in a wooded meadow. Mycol Res 110:734–748

    Article  PubMed  Google Scholar 

  • Thompson M, Calkin DE (2011) Uncertainty and risk in wild land fire management: a review. J Environ Manage 92:1895–0909

    Article  PubMed  Google Scholar 

  • Torres P, Honrubia M (1997) Changes and effects of a natural fire on ectomycorrhizal inoculum potential of soil in a Pinus halepensis forest. For Ecol Manag 96:189–196

    Article  Google Scholar 

  • Treseder KK, Mack MC, Cross A (2004) Relationships among fires, fungi, and soil dynamics in Alaskan boreal forests. Ecol Appl 14:1824–1838

    Article  Google Scholar 

  • Tweig BD, Durall DM, Simard SW (2009) Influence of soil nutrients on ectomycorrhizal communities in a chronosequence of mixed temperate forests. Mycorrhiza 19:305–316

    Article  Google Scholar 

  • Valiente-Banuet A, Verdú M (2007) Facilitation can increase the phylogenetic diversity of plant communities. Ecol Lett 10:1029–1036

    Article  PubMed  Google Scholar 

  • Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505

    Article  Google Scholar 

  • Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098–2100

    Article  CAS  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols—A Guide to Methods and Applications. Academic Press, New York, pp 315–322

    Google Scholar 

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Acknowledgements

We gratefully acknowledge A Carrillo and R Serrada for the aid in fieldwork, and C Mesa, B Cámara and S Pérez-Ortega for their assistance in molecular and phylogenetic analyses. We thank the editor and the anonymous referees for their constructive comments helping to improve the manuscript. This work was founded by the Empresa de Transformación Agraria (TRAGSA), and grants of the Spanish Ministry of Innovation and Science (CGL2011-29585) and the Comunidad de Madrid (S2009/AMB-1511).

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Fig. S1

Map of the study area and location of sampling plots. Two neighbouring areas burned in stand replacing wildfires in the summers of 1994 (Fi-94) (grey plots) and 2005 (Fi-05) (black plots) and an in-between area with a P. pinaster forest unaffected by fire at least in the preceding 60 yr (white plots) were differentiated. Scale 1 cm = 1 km. (PDF 278 kb)

Fig. S2

Phylogenetic tree of the ectomycorrhizal fungi associated with Pinus pinaster seedlings and saplings, in sites differing in the elapsed time since the last fire event: control = > 60 yr after fire (white circles), Fi-94 = 14-yr after fire (squares), and Fi-05 = 3-yr after fire (black triangles). The phylogeny was generated using the 5.8S and 25S LSU sequences of all EM fungal OTUs. The tree was constructed with BEAST programme assuming a general time-reversible model of nucleotide substitution rates, and topological constraints derived from phylogenetic studies of the kingdom Fungi. Black circles point to clades grouping Ascomycetes (up) and Basidiomycetes (down). The scale bar indicates million years. Numbers in parentheses correspond to the identification codes of fungi listed in Table1. (PDF 129 kb)

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Rincón, A., Santamaría, B.P., Ocaña, L. et al. Structure and phylogenetic diversity of post-fire ectomycorrhizal communities of maritime pine. Mycorrhiza 24, 131–141 (2014). https://doi.org/10.1007/s00572-013-0520-0

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