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PMID: 22837398 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape.

Zimmerman NB, Vitousek PM

Abstract

We surveyed endophytic fungal communities in leaves of a single tree species (Metrosideros polymorpha) across wide environmental gradients (500-5,500 mm of rain/y; 10-22 °C mean annual temperature) spanning short geographic distances on Mauna Loa Volcano, Hawai'i. Using barcoded amplicon pyrosequencing at 13 sites (10 trees/site; 10 leaves/tree), we found very high levels of diversity within sites (a mean of 551 ± 134 taxonomic units per site). However, among-site diversity contributed even more than did within-site diversity to the overall richness of more than 4,200 taxonomic units observed in M. polymorpha, and this among-site variation in endophyte community composition correlated strongly with temperature and rainfall. These results are consistent with suggestions that foliar endophytic fungi are hyperdiverse. They further suggest that microbial diversity may be even greater than has been assumed and that broad-scale environmental controls such as temperature and rainfall can structure eukaryotic microbial diversity. Appropriately constrained study systems across strong environmental gradients present a useful means to understand the environmental factors that structure the diversity of microbial communities.

MeSH Terms
Base Sequence Biota Cluster Analysis Computational Biology DNA Primers/genetics Endophytes/genetics,physiology Environment Fungi/genetics,physiology Genetic Variation Geography Hawaii Molecular Sequence Data Myrtaceae/microbiology Plant Leaves/microbiology Rain Sequence Analysis, DNA Species Specificity Temperature
Chemicals
DNA Primers
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Zimmerman Naupaka B
Department of Biology, Stanford University, Stanford, CA 94305, USA. naupaka@stanford.edu
Vitousek Peter M
References (51)
51 references, click to expand
  1. Progressive island colonization and ancient origin of Hawaiian Metrosideros (Myrtaceae).
    Proc Biol Sci. 2008 Jul 7;275(1642):1479-90 PMID: 18426752
  2. Drivers of bacterial beta-diversity depend on spatial scale.
    Proc Natl Acad Sci U S A. 2011 May 10;108(19):7850-4 PMID: 21518859
  3. The Mauna Loa environmental matrix: foliar and soil nutrients.
    Oecologia. 1992 Mar;89(3):372-382 PMID: 28313086
  4. Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots?
    Ecology. 2007 Mar;88(3):541-9 PMID: 17503580
  5. Indoor fungal composition is geographically patterned and more diverse in temperate zones than in the tropics.
    Proc Natl Acad Sci U S A. 2010 Aug 3;107(31):13748-53 PMID: 20616017
  6. Host and geographic structure of endophytic and endolichenic fungi at a continental scale.
    Am J Bot. 2012 May;99(5):898-914 PMID: 22539507
  7. MEGAN analysis of metagenomic data.
    Genome Res. 2007 Mar;17(3):377-86 PMID: 17255551
  8. Genetic structure of the polymorphic metrosideros (Myrtaceae) complex in the Hwaiian islands using nuclear microsatellite data.
    PLoS One. 2009;4(3):e4698 PMID: 19259272
  9. Birch family and environmental conditions affect endophytic fungi in leaves.
    Oecologia. 1999 Feb;118(2):151-156 PMID: 28307689
  10. Wood vessel diameter is related to elevation and genotype in the Hawaiian tree Metrosideros polymorpha (Myrtaceae).
    Am J Bot. 2007 May;94(5):709-15 PMID: 21636440
  11. Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing.
    PLoS Genet. 2008 Nov;4(11):e1000255 PMID: 19023400
  12. Global patterns in belowground communities.
    Ecol Lett. 2009 Nov;12(11):1238-49 PMID: 19674041
  13. Taxonomic reliability of DNA sequences in public sequence databases: a fungal perspective.
    PLoS One. 2006 Dec 20;1:e59 PMID: 17183689
  14. Microbiology of the phyllosphere: a playground for testing ecological concepts.
    Oecologia. 2012 Mar;168(3):621-9 PMID: 21983641
  15. Diversity and evolutionary origins of fungi associated with seeds of a neotropical pioneer tree: a case study for analysing fungal environmental samples.
    Mycol Res. 2009 Apr;113(Pt 4):432-49 PMID: 19103288
  16. Microbiology: Life on leaves.
    Nature. 2009 Oct 8;461(7265):741-2 PMID: 19812663
  17. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities.
    Appl Environ Microbiol. 2009 Dec;75(23):7537-41 PMID: 19801464
  18. PANGEA: pipeline for analysis of next generation amplicons.
    ISME J. 2010 Jul;4(7):852-61 PMID: 20182525
  19. Species delimitation in fungal endophyte diversity studies and its implications in ecological and biogeographic inferences.
    Mol Ecol. 2011 Jul;20(14):3001-13 PMID: 21557783
  20. Potential ecosystem-level effects of genetic variation among populations of Metrosideros polymorpha from a soil fertility gradient in Hawaii.
    Oecologia. 2001 Jan;126(2):266-275 PMID: 28547626
  21. Phylogeography and biogeography of fungi.
    Mycol Res. 2008 Apr;112(Pt 4):423-4 PMID: 18346884
  22. The diversity and biogeography of soil bacterial communities.
    Proc Natl Acad Sci U S A. 2006 Jan 17;103(3):626-31 PMID: 16407148
  23. Diversity, host affinity, and distribution of seed-infecting fungi: a case study with Cecropia.
    Ecology. 2007 Mar;88(3):582-8 PMID: 17503585
  24. Ironing out the wrinkles in the rare biosphere through improved OTU clustering.
    Environ Microbiol. 2010 Jul;12(7):1889-98 PMID: 20236171
  25. A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification?
    Syst Biol. 2009 Jun;58(3):283-97 PMID: 20525584
  26. Eukaryotic microbes, species recognition and the geographic limits of species: examples from the kingdom Fungi.
    Philos Trans R Soc Lond B Biol Sci. 2006 Nov 29;361(1475):1947-63 PMID: 17062413
  27. Hidden fungi, emergent properties: endophytes and microbiomes.
    Annu Rev Phytopathol. 2011;49:291-315 PMID: 19400639
  28. Fungal endophytes: diversity and functional roles.
    New Phytol. 2009;182(2):314-330 PMID: 19236579
  29. Leaf construction cost, nutrient concentration, and net CO2 assimilation of native and invasive species in Hawaii.
    Oecologia. 1999 Nov;121(2):183-192 PMID: 28308558
  30. Canopy cover and leaf age affect colonization by tropical fungal endophytes: Ecological pattern and process in Theobroma cacao (Malvaceae).
    Mycologia. 2003 May-Jun;95(3):388-98 PMID: 21156627
  31. Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist.
    Ecol Lett. 2011 Jan;14(1):19-28 PMID: 21070562
  32. Massively parallel 454-sequencing of fungal communities in Quercus spp. ectomycorrhizas indicates seasonal dynamics in urban and rural sites.
    Mol Ecol. 2010 Mar;19 Suppl 1:41-53 PMID: 20331769
  33. Physiological and morphological variation in Metrosideros polymorpha, a dominant Hawaiian tree species, along an altitudinal gradient: the role of phenotypic plasticity.
    Oecologia. 1998 Jan;113(2):188-196 PMID: 28308196
  34. Microbial diversity in the deep sea and the underexplored "rare biosphere".
    Proc Natl Acad Sci U S A. 2006 Aug 8;103(32):12115-20 PMID: 16880384
  35. Microbial biogeography: putting microorganisms on the map.
    Nat Rev Microbiol. 2006 Feb;4(2):102-12 PMID: 16415926
  36. Removing noise from pyrosequenced amplicons.
    BMC Bioinformatics. 2011 Jan 28;12:38 PMID: 21276213
  37. Geographic locality and host identity shape fungal endophyte communities in cupressaceous trees.
    Mycol Res. 2008 Mar;112(Pt 3):331-44 PMID: 18308531
  38. ESPRIT: estimating species richness using large collections of 16S rRNA pyrosequences.
    Nucleic Acids Res. 2009 Jun;37(10):e76 PMID: 19417062
  39. Insidious effects of sequencing errors on perceived diversity in molecular surveys.
    New Phytol. 2010 Dec;188(4):916-8 PMID: 20854395
  40. PCR: how to kill unwanted DNA.
    Biotechniques. 1992 Mar;12(3):358-60 PMID: 1571142
  41. Multi-scale variation in spatial heterogeneity for microbial community structure in an eastern Virginia agricultural field.
    FEMS Microbiol Ecol. 2003 Jun 1;44(3):335-46 PMID: 12830827
  42. Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR.
    Mycologia. 2007 Mar-Apr;99(2):185-206 PMID: 17682771
  43. The fungi: 1, 2, 3 ... 5.1 million species?
    Am J Bot. 2011 Mar;98(3):426-38 PMID: 21613136
  44. Variation in foliar δ13C in Hawaiian Metrosideros polymorpha: a case of internal resistance?
    Oecologia. 1990 Oct;84(3):362-370 PMID: 28313026
  45. The Ecology and Biogeography of Microorganisms on Plant Surfaces.
    Annu Rev Phytopathol. 2000 Sep;38:145-180 PMID: 11701840
  46. Genetic variation in leaf pigment, optical and photosynthetic function among diverse phenotypes of Metrosideros polymorpha grown in a common garden.
    Oecologia. 2007 Mar;151(3):387-400 PMID: 17124568
  47. Accurate determination of microbial diversity from 454 pyrosequencing data.
    Nat Methods. 2009 Sep;6(9):639-41 PMID: 19668203
  48. QIIME allows analysis of high-throughput community sequencing data.
    Nat Methods. 2010 May;7(5):335-6 PMID: 20383131
  49. Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere.
    New Phytol. 2009 Oct;184(2):438-448 PMID: 19674337
  50. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  51. MUSCLE: multiple sequence alignment with high accuracy and high throughput.
    Nucleic Acids Res. 2004 Mar 19;32(5):1792-7 PMID: 15034147
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2012-08-07
Epub
2012-00-25
Pages
13022-7
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3420199
Subset
IM
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