Plant Host Species and Geographic Distance Affect the Structure of Aboveground Fungal Symbiont Communities, and Environmental Filtering Affects Belowground Communities in a Coastal Dune Ecosystem
详细信息    查看全文
  • 作者:Aaron S. David ; Eric W. Seabloom ; Georgiana May
  • 关键词:Endophyte ; Community assembly ; Environmental drivers ; Dunes ; Ammophila ; Spatial structure
  • 刊名:Microbial Ecology
  • 出版年:2016
  • 出版时间:May 2016
  • 年:2016
  • 卷:71
  • 期:4
  • 页码:912-926
  • 全文大小:768 KB
  • 参考文献:1.Borer ET, Kinkel LL, May G, Seabloom EW (2013) The world within: quantifying the determinants and outcomes of a host’s microbiome. Basic Appl Ecol 14:533–539. doi:10.​1016/​j.​baae.​2013.​08.​009 CrossRef
    2.May G, Nelson P (2014) Defensive mutualisms: do microbial interactions within hosts drive the evolution of defensive traits? Funct Ecol 28:356–363. doi:10.​1111/​1365-2435.​12166 CrossRef
    3.Fierer N, Ferrenberg S, Flores GE et al (2012) From animalcules to an ecosystem: application of ecological concepts to the human microbiome. Annu Rev Ecol Evol Syst 43:137–155. doi:10.​1146/​annurev-ecolsys-110411-160307 CrossRef
    4.Saunders M, Glenn AE, Kohn LM (2010) Exploring the evolutionary ecology of fungal endophytes in agricultural systems: using functional traits to reveal mechanisms in community processes. Evol Appl 3:525–537. doi:10.​1111/​j.​1752-4571.​2010.​00141.​x CrossRef PubMed PubMedCentral
    5.Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Biol 85:183–206. doi:10.​1086/​652373 CrossRef PubMed
    6.Seabloom EW, Borer ET, Gross K, et al (2015) The community ecology of pathogens: coinfection, coexistence and community composition. Ecol Lett 18:401–415. doi:10.​1111/​ele.​12418
    7.Dini-Andreote F, Stegen JC, van Elsas JD, Salles JF (2015) Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc Natl Acad Sci 112:E1326–E1332. doi:10.​1073/​pnas.​1414261112
    8.Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66. doi:10.​1016/​j.​fbr.​2007.​05.​003 CrossRef
    9.Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330. doi:10.​1111/​j.​1469-8137.​2009.​02773.​x CrossRef PubMed
    10.Peay KG, Kennedy PG, Davies SJ, et al (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. doi:10.​1111/​j.​1469-8137.​2009.​03075.​x
    11.Parrent JL, Morris WF, Vilgalys R (2006) CO2-enrichment and nutrient availability alter ectomycorrhizal fungal communities. Ecology 87:2278–2287CrossRef PubMed
    12.Blaalid R, Davey ML, Kauserud H et al (2014) Arctic root-associated fungal community composition reflects environmental filtering. Mol Ecol 23:649–659. doi:10.​1111/​mec.​12622 CrossRef PubMed
    13.Tedersoo L, Bahram M, Toots M et al (2012) Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol Ecol 21:4160–4170. doi:10.​1111/​j.​1365-294X.​2012.​05602.​x CrossRef PubMed
    14.Powell AJ, Parchert KJ, Bustamante JM et al (2012) Thermophilic fungi in an aridland ecosystem. Mycologia 104:813–825. doi:10.​3852/​11-298 CrossRef PubMed
    15.U’Ren JM, Lutzoni F, Miadlikowska J et al (2012) Host and geographic structure of endophytic and endolichenic fungi at a continental scale. Am J Bot 99:898–914. doi:10.​3732/​ajb.​1100459 CrossRef PubMed
    16.Bruns TD, Bidartondo MI, Taylor DL (2002) Host specificity in ectomycorrhizal communities: what do the exceptions tell us? Integr Comp Biol 42:352–359. doi:10.​1093/​icb/​42.​2.​352 CrossRef PubMed
    17.Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340. doi:10.​1146/​annurev.​arplant.​55.​031903.​141735 CrossRef PubMed
    18.Terborgh J, Alvarez-Loayza P, Dexter K et al (2011) Decomposing dispersal limitation: limits on fecundity or seed distribution? J Ecol 99:935–944. doi:10.​1111/​j.​1365-2745.​2011.​01836.​x CrossRef
    19.Ettema CH, Wardle DA (2002) Spatial soil ecology. Trends Ecol Evol 17:177–183. doi:10.​1016/​S0169-5347(02)02496-5 CrossRef
    20.Peay KG, Bruns TD, Kennedy PG et al (2007) A strong species-area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi. Ecol Lett 10:470–480. doi:10.​1111/​j.​1461-0248.​2007.​01035.​x CrossRef PubMed
    21.Talbot JM, Bruns TD, Taylor JW et al (2014) Endemism and functional convergence across the North American soil mycobiome. Proc Natl Acad Sci U S A 111:6341–6346. doi:10.​1073/​pnas.​1402584111 CrossRef PubMed PubMedCentral
    22.Baas-Becking L (1934) Geobiologie of inleiding tot de milieukunde. W.P. Van Stockum & Zoon N.V., The Hague, Netherlands
    23.Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:497–506. doi:10.​1038/​nrmicro2795 PubMed
    24.Beck S, Powell JR, Drigo B et al (2015) The role of stochasticity differs in the assembly of soil- and root-associated fungal communities. Soil Biol Biochem 80:18–25. doi:10.​1016/​j.​soilbio.​2014.​09.​010 CrossRef
    25.Costello EK, Lauber CL, Hamady M et al (2009) Bacterial community variation in human body habitats across space and time. Science 326:1694–1697. doi:10.​1126/​science.​1177486 CrossRef PubMed PubMedCentral
    26.Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews JH, Hirano S (eds) Microb ecol. leaves. Springer, New York, pp 179–197CrossRef
    27.Coince A, Cordier T, Lengellé J et al (2014) Leaf and root-associated fungal assemblages do not follow similar elevational diversity patterns. PLoS One 9, e100668. doi:10.​1371/​journal.​pone.​0100668 CrossRef PubMed PubMedCentral
    28.Ridaura VK, Faith JJ, Rey FE et al (2013) Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341:1241214. doi:10.​1126/​science.​1241214 CrossRef PubMed
    29.Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190:783–793. doi:10.​1111/​j.​1469-8137.​2010.​03611.​x CrossRef PubMed
    30.Kivlin SN, Winston GC, Goulden ML, Treseder KK (2014) Environmental filtering affects soil fungal community composition more than dispersal limitation at regional scales. Fungal Ecol 12:14–25. doi:10.​1016/​j.​funeco.​2014.​04.​004 CrossRef
    31.Gilbert GS, Reynolds DR (2005) Nocturnal fungi: airborne spores in the canopy and understory of a tropical rain forest. Biotropica 37:462–464. doi:10.​1111/​j.​1744-7429.​2005.​00061.​x CrossRef
    32.Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43:2294–2303. doi:10.​1016/​j.​soilbio.​2011.​07.​012 CrossRef
    33.Hacker SD, Zarnetske P, Seabloom E et al (2012) Subtle differences in two non-native congeneric beach grasses significantly affect their colonization, spread, and impact. Oikos 121:138–148. doi:10.​1111/​j.​1600-0706.​2011.​18887.​x CrossRef
    34.Zarnetske PL, Seabloom EW, Hacker SD (2010) Non-target effects of invasive species management: beachgrass, birds, and bulldozers in coastal dunes. Ecosphere 1:art13. doi:10.​1890/​ES10-00101.​1
    35.Seabloom EW, Ruggiero P, Hacker SD et al (2013) Invasive grasses, climate change, and exposure to storm-wave overtopping in coastal dune ecosystems. Glob Chang Biol 19:824–832. doi:10.​1111/​gcb.​12078 CrossRef PubMed
    36.David AS, Zarnetske PL, Hacker SD et al (2015) Invasive congeners differ in successional impacts across space and time. PLoS One 10, e0117283. doi:10.​1371/​journal.​pone.​0117283 CrossRef PubMed PubMedCentral
    37.Cooper WS (1958) Coastal sand dunes. Geological Society of America, Memoir 72, Boulder, Coliorado
    38.Arnold AE, Henk DA, Eells RL et al (2007) Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia 99:185–206CrossRef PubMed
    39.Gardes M, Bruns T (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118CrossRef PubMed
    40.Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246.
    41.Kearse M, Moir R, Wilson A, et al (2012) Geneious. Bioinformatics 28:1647–1649. doi:10.​1093/​bioinformatics/​bts199
    42.Monacell JT, Carbone I (2014) Mobyle SNAP Workbench: a web-based analysis portal for population genetics and evolutionary genomics. Bioinformatics 30:1–3. doi:10.​1093/​bioinformatics/​btu055 CrossRef
    43.Nilsson RH, Veldre V, Hartmann M et al (2010) An open source software package for automated extraction of ITS1 and ITS2 from fungal ITS sequences for use in high-throughput community assays and molecular ecology. Fungal Ecol 3:284–287. doi:10.​1016/​j.​funeco.​2010.​05.​002 CrossRef
    44.Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing MOTHUR: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi:10.​1128/​AEM.​01541-09 CrossRef PubMed PubMedCentral
    45.Sun Y, Cai Y, Liu L et al (2009) ESPRIT: estimating species richness using large collections of 16 rRNA pyrosequences. Nucleic Acids Res 37:1–13. doi:10.​1093/​nar/​gkp285 CrossRef
    46.R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://​www.​R-project.​org/​ . R Found. Stat. Comput. Vienna, Austria
    47.David AS, Seabloom EW, May G (2015) Fungal endophytes of pacific northwest beachgrasses dataset. Data Repos Univ Minnesota. doi:10.​13020/​D68G60
    48.Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–51
    49.Burnham KP, Anderson DR (2002) Model selection and multimodel inference. Technometrics. doi:10.​1198/​tech.​2003.​s146
    50.Barton K (2014) MuMIn: multi-model inference. R package version. 1.12.1. http://​CRAN.​R-project.​org/​package=​MuMIn
    51.Oksanen J, Blanchet FG, Kindt R et al (2013) Package “vegan”. R Packag ver 20–8:254
    52.Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19CrossRef
    53.Fox J, Weisberg S (2011) Nonlinear regression and nonlinear least squares in R. Sage, Thousand Oaks
    54.Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140:295–310. doi:10.​1046/​j.​1469-8137.​1998.​00265.​x CrossRef
    55.Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 53:173–189. doi:10.​3114/​sim.​53.​1.​173 CrossRef
    56.Mandyam K, Loughin T, Jumpponen A (2010) Isolation and morphological and metabolic characterization of common endophytes in annually burned tallgrass prairie. Mycologia 102:813–821. doi:10.​3852/​09-212 CrossRef PubMed
    57.Yatsunenko T, Rey FE, Manary MJ et al (2012) Human gut microbiome viewed across age and geography. Nature 486:222–227. doi:10.​1038/​nature11053 PubMed PubMedCentral
    58.Botnen S, Vik U, Carlsen T et al (2014) Low host specificity of root-associated fungi at an Arctic site. Mol Ecol 23:975–985. doi:10.​1111/​mec.​12646 CrossRef PubMed
    59.Tejesvi MV, Ruotsalainen AL, Markkola AM, Pirttilä AM (2010) Root endophytes along a primary succession gradient in northern Finland. Fungal Divers 41:125–134. doi:10.​1007/​s13225-009-0016-6 CrossRef
    60.Caldwell BA, Jumpponen A, Trappe JM (2000) Mycological Society of America utilization of major detrital substrates by dark-septate, root endophytes. Mycologia 92:230–232. doi:10.​2307/​3761555 CrossRef
    61.Jumpponen A, Mattson KG, Trappe JM (1998) Mycorrhizal functioning of Phialocephala fortinii with Pinus contorta on glacier forefront soil: interactions with soil nitrogen and organic matter. Mycorrhiza 7:261–265. doi:10.​1007/​s005720050190 CrossRef PubMed
    62.Higgins KL, Arnold AE, Coley PD, Kursar T (2014) Communities of fungal endophytes in tropical forest grasses: highly diverse host- and habitat generalists characterized by strong spatial structure. Fungal Ecol 8:1–11. doi:10.​1016/​j.​funeco.​2013.​12.​005 CrossRef
    63.Mitchell C, Tilman D, Groth J (2002) Effects of grassland plant species diversity, abundance, and composition on foliar fungal disease. Ecology 83:1713–1726CrossRef
    64.Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk. Ecol Lett 9:485–498. doi:10.​1111/​j.​1461-0248.​2006.​00885.​x CrossRef PubMed
    65.Zarnetske PL, Hacker SD, Seabloom EW et al (2012) Biophysical feedback mediates effects of invasive grasses on coastal dune shape. Ecology 93:1439–1450CrossRef PubMed
    66.Ogura A, Yura H (2008) Effects of sandblasting and salt spray on inland plants transplanted to coastal sand dunes. Ecol Res 23:107–112. doi:10.​1007/​s11284-007-0347-2 CrossRef
    67.Glassman SI, Peay KG, Talbot JM, et al (2015) A continental view of pine-associated ectomycorrhizal fungal spore banks: a quiescent functional guild with a strong biogeographic pattern. New Phytol 205:167–181. doi:10.​1111/​nph.​13240
    68.Rodriguez RJ, Henson J, Van Volkenburgh E et al (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416. doi:10.​1038/​ismej.​2007.​106 CrossRef PubMed
    69.Emery SM, Thompson D, Rudgers JA (2010) Variation in endophyte symbiosis, herbivory and drought tolerance of Ammophila breviligulata populations in the Great Lakes region. Am Midl Nat 163:186–196. doi:10.​1674/​0003-0031-163.​1.​186 CrossRef
    70.Beckstead J, Parker I (2003) Invasiveness of Ammophila arenaria: release from soil-borne pathogens? Ecology 84:2824–2831CrossRef
    71.Mandyam KG, Roe J, Jumpponen A (2013) Arabidopsis thaliana model system reveals a continuum of responses to root endophyte colonization. Fungal Biol 117:250–260. doi:10.​1016/​j.​funbio.​2013.​02.​001 CrossRef PubMed
  • 作者单位:Aaron S. David (1)
    Eric W. Seabloom (1)
    Georgiana May (1) (2)

    1. Department of Ecology, Evolution, and Behavior, University of Minnesota, 1479 Gortner Avenue, Saint Paul, MN, 55108, USA
    2. Department of Plant Biology, University of Minnesota, 1479 Gortner Avenue, Saint Paul, MN, 55108, USA
  • 刊物类别:Biomedical and Life Sciences
  • 刊物主题:Life Sciences
    Microbiology
    Ecology
    Geoecology and Natural Processes
    Nature Conservation
  • 出版者:Springer New York
  • ISSN:1432-184X
文摘
Microbial symbionts inhabit tissues of all plants and animals. Their community composition depends largely on two ecological processes: (1) filtering by abiotic conditions and host species determining the environments that symbionts are able to colonize and (2) dispersal-limitation determining the pool of symbionts available to colonize a given host and community spatial structure. In plants, the above- and belowground tissues represent such distinct habitats for symbionts that we expect different effects of filtering and spatial structuring on their symbiont communities. In this study, we characterized above- and belowground communities of fungal endophytes—fungi living asymptomatically within plants—to understand the contributions of filtering and spatial structure to endophyte community composition. We used a culture-based approach to characterize endophytes growing in leaves and roots of three species of coastal beachgrasses in dunes of the USA Pacific Northwest. For leaves, endophyte isolation frequency and OTU richness depended primarily on plant host species. In comparison, for roots, both isolation frequency and OTU richness increased from the nutrient-poor front of the dune to the higher-nutrient backdune. Endophyte community composition in leaves exhibited a distance-decay relationship across the region. In a laboratory assay, faster growth rates and lower spore production were more often associated with leaf- than root-inhabiting endophytes. Overall, our results reveal a greater importance of biotic filtering by host species and dispersal-limitation over regional geographic distances for aboveground leaf endophyte communities and stronger effects of abiotic environmental filtering and locally patchy distributions for belowground root endophyte communities.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700