Original Article

Microbial Ecology and Functional Diversity of Natural Habitats

Strong coupling of plant and fungal community structure across western Amazonian rainforests

  • The ISME Journal (2013) 7, 18521861 (2013)
  • doi:10.1038/ismej.2013.66
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Abstract

The Amazon basin harbors a diverse ecological community that has a critical role in the maintenance of the biosphere. Although plant and animal communities have received much attention, basic information is lacking for fungal or prokaryotic communities. This is despite the fact that recent ecological studies have suggested a prominent role for interactions with soil fungi in structuring the diversity and abundance of tropical rainforest trees. In this study, we characterize soil fungal communities across three major tropical forest types in the western Amazon basin (terra firme, seasonally flooded and white sand) using 454 pyrosequencing. Using these data, we examine the relationship between fungal diversity and tree species richness, and between fungal community composition and tree species composition, soil environment and spatial proximity. We find that the fungal community in these ecosystems is diverse, with high degrees of spatial variability related to forest type. We also find strong correlations between α- and β-diversity of soil fungi and trees. Both fungal and plant community β-diversity were also correlated with differences in environmental conditions. The correlation between plant and fungal richness was stronger in fungal lineages known for biotrophic strategies (for example, pathogens, mycorrhizas) compared with a lineage known primarily for saprotrophy (yeasts), suggesting that this coupling is, at least in part, due to direct plant–fungal interactions. These data provide a much-needed look at an understudied dimension of the biota in an important ecosystem and supports the hypothesis that fungal communities are involved in the regulation of tropical tree diversity.

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References

  1. , , , . (2010). Indoor fungal composition is geographically patterned and more diverse in temperate zones than in the tropics. Proc Natl Aacd Sci USA 107: 13748–13753.

  2. . (2001). A new method for non-parametric multivariate analysis of variance. Aust Ecol 26: 32–46.

  3. , . (2007). Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88: 541–549.

  4. , , , , , et al (2003). Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA 100: 15649–15654.

  5. . (1983). Seed dispersal of the tropical tree, Platypodium elegans, and the escape of its seedlings from fungal pathogens. J Ecol 71: 759–771.

  6. , , , , , et al (2011). Disentangling stand and environmental correlates of aboveground biomass in Amazonian forests. Global Change Biol 17: 2677–2688.

  7. . (2001). The phylogeny of plant and animal pathogens in the Ascomycota. Physiol Mol Plant Pathol 59: 165–187.

  8. . (2002). Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proc R Soc B 269: 2595–2601.

  9. . (1943). Geographical distribution of fungi. Bot Rev 9: 466–482.

  10. . (2010). Serpentine soils promote ectomycorrhizal fungal diversity. Mol Ecol 19: 5566–5576.

  11. , , , , , et al (2009). 454 Pyrosequencing analyses of forest soils reveals an unexpectedly high fungal diversity. New Phytologist 184: 449–456.

  12. , , , , , et al (2010). QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335–336.

  13. , , , . (2010). Asymmetric density dependence shapes species abundances in a tropical tree community. Science 329: 330–332.

  14. . (1971). On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: Den Boer PJ, Gradwell GR, (eds). Dynamics of Populations. PUDOC: Wageningen, the Netherlands, pp 298–312.

  15. . (1978). Diversity in tropical rain forests and coral reefs—high diversity of trees and corals is maintained only in a non-equilibrium state. Science 199: 1302–1310.

  16. , . (2008). Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin. Curr Opin Microbiol 11: 525–531.

  17. , , , , . (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194–2200.

  18. . (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460–2461.

  19. , . (2010). Phylogenetic similarity and structure of Agaricomycotina communities across a forested landscape. Mol Ecol 19: 1469–1482.

  20. , , . (2008). The microbial engines that drive Earth’s biogeochemical cycles. Science 320: 1034–1039.

  21. , . (2012). Taxa-area relationship and neutral dynamics influence the diversity of fungal communities on senesced tree leaves. Environ Microbiol 14: 1488–1499.

  22. , , , , . (2010). A floristic study of the white-sand forests of Peru. Ann Missouri Botanical Garden 97: 283–305.

  23. , . (2011). Phylogenetic community structure and phylogenetic turnover across space and edaphic gradients in western Amazonian tree communities. Ecography 34: 552–565.

  24. . (2002). Global dispersal of free-living microbial eukaryote species. Science 296: 1061–1063.

  25. , , , , , . (2011). Microbially mediated plant functional traits. Annu Rev Ecol Evol Systematics 42: 23–46.

  26. , , . (2011). 95% of basidiospores fall within one meter of the cap- a field and modeling based study. Mycologia 103: 1175–1183.

  27. , . (1993). ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2: 113–118.

  28. . (2000). Global patterns in biodiversity. Nature 405: 220–227.

  29. , , . (2002). Polypore fungal diversity and host density in a moist tropical forest. Biodiversity Conservation 11: 947–957.

  30. , . (2002). Host specialization among wood-decay polypore fungi in a Caribbean mangrove forest. Biotropica 34: 396–404.

  31. , . (2007). Phylogenetic signal in plant pathogen-host range. PNAS 104: 4979–4983.

  32. . (2002). Evolutionary ecology of plant diseases in natural ecosystems. Annu Rev Phytopathol 40: 13–43.

  33. . (1962). Pest pressure, an underestimated factor in evolution. Systematics Assoc Publ 4: 37–46.

  34. , , , , , et al (2004). Spatial scaling of microbial eukaryote diversity. Nature 432: 747–750.

  35. , , , , , et al (2007). Tropical forests and climate policy. Science 316: 985–986.

  36. , . (2000). Phellinus weirii and other native root pathogens as determinants of forest structure and process in western North America. Annu Rev Phytopathol 38: 515–539.

  37. , , , , . (2000). Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature 404: 493–495.

  38. . (1991). The fungal dimension of biodiversity—magnitude, significance and conservation. Mycol Res 95: 641–655.

  39. . (2012). Global species numbers of fungi: are tropical studies and molecular approaches contributing to a more robust estimate? Biodiversity Conservation 21: 2425–2433.

  40. , , . (2002). Ectomycorrhizal fungi and their leguminous hosts in the Pakaraima Mountains of Guyana. Mycol Res 106: 515–531.

  41. , , , . (2004). A taxa-area relationship for bacteria. Nature 432: 750–753.

  42. . (2001) The Unified Neutral Theory of Biodiversity and Biogeography. Princeton University Press: Princeton, NJ, USA.

  43. , , , , , et al (2012). New primers to amplify the fungal ITS2 region—evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol Ecol 82: 666–677.

  44. , , . (2005). Detection of plot-level changes in ectomycorrhizal communities across years in an old-growth mixed-conifer forest. New Phytologist 166: 619–630.

  45. . (1970). Herbivores and the number of tree species in tropical forests. Am Nat 104: 501–528.

  46. . (2002). Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417: 67–70.

  47. , . (2010). Denoising pyrosequencing reads by flowgram clustering. Nat Methods 7: 668–669.

  48. , , . (2003). Measuring beta diversity for presence-absence data. J Anim Ecol 72: 367–382.

  49. , , , , , . (2012). Experimental evidence for a phylogenetic Janzen–Connell effect in a subtropical forest. Ecol Lett 15: 111–118.

  50. , , , , , et al (2010). Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466: 752–755.

  51. . (1998). Climatologia de la zona de Iquito, Peru. In: Kailliola R, Flores Paitan S, Geoecologia y desarrollo Amazonico: estudio integrado en la zona de Iquitos, Peru. University of Turku Press: Turku, pp 35–57.

  52. . (1991). A fondness for fungi. Nature 352: 475–476.

  53. , , , , . (2012). Fungal community composition in neotropical rain forests: the influence of tree diversity and precipitation. Microb Ecol 63: 804–812.

  54. , , . (2008). Fungal community ecology: a hybrid beast with a molecular master. BioScience 58: 799–810.

  55. , , , , . (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 Phytologist 185: 529–542.

  56. , , , . (2012). Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol Ecol 16: 4122–4136.

  57. , , , , , et al (2003). Habitat association among Amazonian tree species: a landscape-scale approach. J Ecol 91: 757–775.

  58. , , , , . (2011). No biogeographical pattern for a root-associated fungal species complex. Global Ecol Biogeography 20: 160–169.

  59. R Core Development Team (2009) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria.

  60. , , . (2007). Intra-specific and intra-sporocarp ITS variation of ectomycorrhizal fungi as assessed by rDNA sequencing of sporocarps and pooled ectomycorrhizal roots from a Quercus woodland. Mycorrhiza 18: 15–22.

  61. , , , , . (2011). Ectomycorrhizal fungal diversity and community structure on three co-occurring leguminous canopy tree species in a Neotropical rainforests. New Phytologist 192: 699–712.

  62. , , , , , . (2013). The ectomycorrhizal fungal community in a Neotropical forest dominated by the endemic dipterocarp Pakaraimaea dipterocarpacea. PLoS One 8: e55160.

  63. , . (2008) Mycorrhizal Symbiosis 3rd edn. Elsevier: San Francisco, CA, USA.

  64. , , , . (2006). Phylogenetics of Saccharomycetales, the ascomycete yeasts. Mycologia 98: 1006–1017.

  65. , , , , , et al (2012). Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol Ecol 21: 4160–4170.

  66. , , , , , et al (2010). 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytologist 188: 291–301.

  67. . (2012). Enemies maintain hyperdiverse tropical forests. Am Nat 179: 303–314.

  68. , , , . (2012). High-coverage ITS primers for the DNA-based identification of Ascomycetes and Basidiomycetes in environmental samples. PLoS ONE 7: e40863.

  69. , , . (2003). Dispersal, environment, and floristic variation of western Amazonian forests. Science 299: 241–244.

  70. , , , , , et al (1998). Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69–72.

  71. , , , , . (2006). Resource availability controls fungal diversity across a plant diversity gradient. Ecol Lett 9: 1127–1135.

  72. . (2002). Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130: 1–14.

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Acknowledgements

Support for KGP was provided by the National Science Foundation Grant DBI 1045658 and for PVAF and CB by a collaborative NSF Grant DEB-0743800/0743103. We thank Italo Mesones, Julio Sanchez, Julio Grandez Ríos, Tracy Misiewicz, Seth Kauppinen and Fabio Casado for help in field work and comments on previous versions of this manuscript.

Author information

Affiliations

  1. Department of Biology, Stanford University, Stanford, CA, USA

    • Kabir G Peay
  2. INRA, UMR Écologie des Forêts de Guyane, Kourou, French Guiana, France

    • Christopher Baraloto
  3. Department of Integrative Biology, University of California, Berkeley, CA, USA

    • Paul VA Fine

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Competing interests

The authors declare no conflict of interest.

Corresponding author

Correspondence to Kabir G Peay.

Supplementary information