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Title: Carbon constrains fungal endophyte assemblages along the timberline

Abstract

Summary The alpha diversity of foliar fungal endophytes ( FEs ) in leaves of B etula ermanii in a subalpine timberline ecotone on C hangbai M ountain, C hina increased with elevation. There were also significant differences in beta diversity along the elevation gradient. Among the environmental variables analysed, leaf carbon significantly increased with elevation, and was the most significant environmental factor that constrained the alpha and beta diversity in the FE communities. Tree height and the cellulose, lignin, and carbon/nitrogen ratio of the leaves also affected the FE assemblages. When controlled for the effects of elevation, leaf carbon was still the main driver of changes in evenness, Shannon diversity and FE community composition. The results offered clues of the carbon acquisition strategy of the foliar FEs across this cold terrain. There was strong multicollinearity between both annual precipitation and temperature, with elevation (| P earson r| > 0.986), so the effects of these climatic variables were impossible to separate; however, they may play key roles, and the direct effects of both warrant further investigation. As pioneer decomposers of leaf litter, variations in diversity and community composition of FE measured here may feedback and influence carbon cycling and dynamics in these forestmore » ecosystems.« less

Authors:
 [1];  [2];  [3];  [4];  [1];  [4];  [4]
  1. State Key Laboratory of Soil and Sustainable Agriculture Institute of Soil Science Chinese Academy of Sciences 71 East Beijing Road Nanjing 210008 China, University of Chinese Academy of Sciences Beijing 100049 China
  2. Argonne National Laboratory Institute for Genomics and Systems Biology Argonne IL 60439 USA
  3. Argonne National Laboratory Institute for Genomics and Systems Biology Argonne IL 60439 USA, Departments of Ecology and Evolution, Surgery University of Chicago Chicago IL 60637 USA, Marine Biological Laboratory 7 MBL Street Woods Hole MA 02543 USA, College of Environmental and Resource Sciences Zhejiang University Hangzhou 310058 China
  4. State Key Laboratory of Soil and Sustainable Agriculture Institute of Soil Science Chinese Academy of Sciences 71 East Beijing Road Nanjing 210008 China
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1401174
Grant/Contract Number:  
DE‐AC02‐06CH11357
Resource Type:
Publisher's Accepted Manuscript
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Name: Environmental Microbiology Journal Volume: 18 Journal Issue: 8; Journal ID: ISSN 1462-2912
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Yang, Teng, Weisenhorn, Pamela, Gilbert, Jack A., Ni, Yingying, Sun, Ruibo, Shi, Yu, and Chu, Haiyan. Carbon constrains fungal endophyte assemblages along the timberline. United Kingdom: N. p., 2016. Web. doi:10.1111/1462-2920.13153.
Yang, Teng, Weisenhorn, Pamela, Gilbert, Jack A., Ni, Yingying, Sun, Ruibo, Shi, Yu, & Chu, Haiyan. Carbon constrains fungal endophyte assemblages along the timberline. United Kingdom. https://doi.org/10.1111/1462-2920.13153
Yang, Teng, Weisenhorn, Pamela, Gilbert, Jack A., Ni, Yingying, Sun, Ruibo, Shi, Yu, and Chu, Haiyan. Mon . "Carbon constrains fungal endophyte assemblages along the timberline". United Kingdom. https://doi.org/10.1111/1462-2920.13153.
@article{osti_1401174,
title = {Carbon constrains fungal endophyte assemblages along the timberline},
author = {Yang, Teng and Weisenhorn, Pamela and Gilbert, Jack A. and Ni, Yingying and Sun, Ruibo and Shi, Yu and Chu, Haiyan},
abstractNote = {Summary The alpha diversity of foliar fungal endophytes ( FEs ) in leaves of B etula ermanii in a subalpine timberline ecotone on C hangbai M ountain, C hina increased with elevation. There were also significant differences in beta diversity along the elevation gradient. Among the environmental variables analysed, leaf carbon significantly increased with elevation, and was the most significant environmental factor that constrained the alpha and beta diversity in the FE communities. Tree height and the cellulose, lignin, and carbon/nitrogen ratio of the leaves also affected the FE assemblages. When controlled for the effects of elevation, leaf carbon was still the main driver of changes in evenness, Shannon diversity and FE community composition. The results offered clues of the carbon acquisition strategy of the foliar FEs across this cold terrain. There was strong multicollinearity between both annual precipitation and temperature, with elevation (| P earson r| > 0.986), so the effects of these climatic variables were impossible to separate; however, they may play key roles, and the direct effects of both warrant further investigation. As pioneer decomposers of leaf litter, variations in diversity and community composition of FE measured here may feedback and influence carbon cycling and dynamics in these forest ecosystems.},
doi = {10.1111/1462-2920.13153},
journal = {Environmental Microbiology},
number = 8,
volume = 18,
place = {United Kingdom},
year = {Mon Jan 18 00:00:00 EST 2016},
month = {Mon Jan 18 00:00:00 EST 2016}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/1462-2920.13153

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Cited by: 27 works
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Works referenced in this record:

UCHIME improves sensitivity and speed of chimera detection
journal, June 2011


Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist: Roadmap for beta diversity
journal, November 2010


Effects of Elevated Carbon Dioxide and Ozone on Foliar Proanthocyanidins in Betula platyphylla, Betula ermanii, and Fagus crenata Seedlings
journal, May 2006

  • Karonen, Maarit; Ossipov, Vladimir; Ossipova, Svetlana
  • Journal of Chemical Ecology, Vol. 32, Issue 7
  • DOI: 10.1007/s10886-006-9061-8

Fungal Taxa Target Different Carbon Sources in Forest Soil
journal, September 2008


Key canopy traits drive forest productivity
journal, January 2012

  • Reich, Peter B.
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 279, Issue 1736
  • DOI: 10.1098/rspb.2011.2270

Contrasting elevational diversity patterns between eukaryotic soil microbes and plants
journal, November 2014

  • Shen, Congcong; Liang, Wenju; Shi, Yu
  • Ecology, Vol. 95, Issue 11
  • DOI: 10.1890/14-0310.1

Fungal Communities Respond to Long-Term CO 2 Elevation by Community Reassembly
journal, January 2015

  • Tu, Qichao; Yuan, Mengting; He, Zhili
  • Applied and Environmental Microbiology, Vol. 81, Issue 7
  • DOI: 10.1128/AEM.04040-14

Host and geographic structure of endophytic and endolichenic fungi at a continental scale
journal, May 2012

  • U'Ren, Jana M.; Lutzoni, François; Miadlikowska, Jolanta
  • American Journal of Botany, Vol. 99, Issue 5
  • DOI: 10.3732/ajb.1100459

A comparison of methods for determining proximate carbon fractions of forest litter
journal, February 1990

  • Ryan, Michael G.; Melillo, Jerry M.; Ricca, Andrea
  • Canadian Journal of Forest Research, Vol. 20, Issue 2
  • DOI: 10.1139/x90-023

Ion Torrent PGM as Tool for Fungal Community Analysis: A Case Study of Endophytes in Eucalyptus grandis Reveals High Taxonomic Diversity
journal, December 2013


Fungal endophytes: diversity and functional roles
journal, February 2009


Endophytic fungi associated with cacti in Arizona
journal, May 2005

  • Suryanarayanan, Trichur S.; Wittlinger, Sally K.; Faeth, Stanley H.
  • Mycological Research, Vol. 109, Issue 5
  • DOI: 10.1017/S0953756205002753

Hidden Fungi, Emergent Properties: Endophytes and Microbiomes
journal, September 2011


The composition of phyllosphere fungal assemblages of E uropean beech ( F agus sylvatica ) varies significantly along an elevation gradient
journal, August 2012


Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007

  • Wang, Q.; Garrity, G. M.; Tiedje, J. M.
  • Applied and Environmental Microbiology, Vol. 73, Issue 16
  • DOI: 10.1128/AEM.00062-07

Endophytic fungi in European aspen (Populus tremula) leaves—diversity, detection, and a suggested correlation with herbivory resistance
journal, January 2010

  • Albrectsen, Benedicte R.; Björkén, Lars; Varad, Akkamahadevi
  • Fungal Diversity, Vol. 41, Issue 1
  • DOI: 10.1007/s13225-009-0011-y

Bleaching of leaf litter and associated microfungi in subboreal and subalpine forests
journal, October 2015

  • Hagiwara, Yusuke; Matsuoka, Shunsuke; Hobara, Satoru
  • Canadian Journal of Microbiology, Vol. 61, Issue 10
  • DOI: 10.1139/cjm-2015-0111

The UNITE database for molecular identification of fungi - recent updates and future perspectives: Letters
journal, March 2010


Interactions of two endophytic fungi colonizing Atractylodes lancea and effects on the host’s essential oils
journal, April 2013


Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain
journal, February 2013


Soil-Borne Bacterial Structure and Diversity Does Not Reflect Community Activity in Pampa Biome
journal, October 2013

  • Lupatini, Manoeli; Suleiman, Afnan Khalil Ahmad; Jacques, Rodrigo Josemar Seminoti
  • PLoS ONE, Vol. 8, Issue 10
  • DOI: 10.1371/journal.pone.0076465

Altitudinal and seasonal variation of frost resistance of Fagus crenata and Betula ermanii along the Pacific slope of Mt. Fuji, Japan
journal, June 1999


Community composition of endophytic fungi in Acer truncatum and their role in decomposition
journal, January 2011


Fungal endophytes limit pathogen damage in a tropical tree
journal, December 2003

  • Arnold, A. E.; Mejia, L. C.; Kyllo, D.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 26
  • DOI: 10.1073/pnas.2533483100

Factors influencing limit values for pine needle litter decomposition: a synthesis for boreal and temperate pine forest systems
journal, February 2010


Diversity and host Range of Foliar Fungal Endophytes: are Tropical Leaves Biodiversity Hotspots?
journal, March 2007

  • Arnold, A. Elizabeth; Lutzoni, F.
  • Ecology, Vol. 88, Issue 3
  • DOI: 10.1890/05-1459

Low host specificity of root-associated fungi at an Arctic site
journal, January 2014

  • Botnen, Synnøve; Vik, Unni; Carlsen, Tor
  • Molecular Ecology, Vol. 23, Issue 4
  • DOI: 10.1111/mec.12646

Search and clustering orders of magnitude faster than BLAST
journal, August 2010


Relocation, high-latitude warming and host genetic identity shape the foliar fungal microbiome of poplars
journal, December 2014

  • Bálint, Miklós; Bartha, László; O'Hara, Robert B.
  • Molecular Ecology, Vol. 24, Issue 1
  • DOI: 10.1111/mec.13018

Phylogenetic relationships, host affinity, and geographic structure of boreal and arctic endophytes from three major plant lineages
journal, February 2007

  • Higgins, K. Lindsay; Arnold, A. Elizabeth; Miadlikowska, Jolanta
  • Molecular Phylogenetics and Evolution, Vol. 42, Issue 2
  • DOI: 10.1016/j.ympev.2006.07.012

Amplicon-pyrosequencing-based detection of compositional shifts in bryophyte-associated fungal communities along an elevation gradient
journal, November 2012

  • Davey, Marie L.; Heegaard, Einar; Halvorsen, Rune
  • Molecular Ecology, Vol. 22, Issue 2
  • DOI: 10.1111/mec.12122

Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates
journal, January 2010


Cross-biome metagenomic analyses of soil microbial communities and their functional attributes
journal, December 2012

  • Fierer, N.; Leff, J. W.; Adams, B. J.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 52
  • DOI: 10.1073/pnas.1215210110

Altitudinal distribution of microfungi associated with Betula ermanii leaf litter on Mt. Rishiri, northern Japan
journal, July 2009

  • Osono, Takashi; Hirose, Dai
  • Canadian Journal of Microbiology, Vol. 55, Issue 7
  • DOI: 10.1139/W09-030

Degradation of cellulose by basidiomycetous fungi
journal, May 2008


Studies on the incidence of coniferous needle endophytes in the Pacific Northwest
journal, December 1978

  • Carroll, George C.; Carroll, Fanny E.
  • Canadian Journal of Botany, Vol. 56, Issue 24
  • DOI: 10.1139/b78-367

Fungal community on decomposing leaf litter undergoes rapid successional changes
journal, October 2012


Simulating forest ecosystem response to climate warming incorporating spatial effects in north-eastern China
journal, December 2005


Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions
journal, September 2010


ITS1 versus ITS2 as DNA metabarcodes for fungi
journal, January 2013

  • Blaalid, R.; Kumar, S.; Nilsson, R. H.
  • Molecular Ecology Resources, Vol. 13, Issue 2
  • DOI: 10.1111/1755-0998.12065

Climatic factors affecting the tree-ring width of Betula ermanii at the timberline on Mount Norikura, central Japan
journal, May 2005


Why are there global gradients in species richness? mountains might hold the answer
journal, December 2000


Microbes on mountainsides: Contrasting elevational patterns of bacterial and plant diversity
journal, August 2008

  • Bryant, J. A.; Lamanna, C.; Morlon, H.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue Supplement 1
  • DOI: 10.1073/pnas.0801920105

High consistency between replicate 454 pyrosequencing analyses of ectomycorrhizal plant root samples
journal, July 2011


Distinct soil bacterial communities along a small-scale elevational gradient in alpine tundra
journal, June 2015


Are tropical fungal endophytes hyperdiverse?
journal, July 2000


Summer temperature variations in southern Kamchatka as reconstructed from a 247-year tree-ring chronology of Betula ermanii
journal, August 2010


Contrasting patterns in elevational diversity between microorganisms and macroorganisms: Patterns in elevational diversity
journal, November 2010


Leaf-inhabiting endophytic fungi of European Beech (Fagus sylvatica L.) co-occur in leaf litter but are rare on decaying wood of the same host
journal, February 2013


Basic local alignment search tool
journal, October 1990

  • Altschul, Stephen F.; Gish, Warren; Miller, Webb
  • Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
  • DOI: 10.1016/S0022-2836(05)80360-2

QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

Climate affects symbiotic fungal endophyte diversity and performance
journal, July 2013

  • Giauque, Hannah; Hawkes, Christine V.
  • American Journal of Botany, Vol. 100, Issue 7
  • DOI: 10.3732/ajb.1200568

Endophytic fungi: resource for gibberellins and crop abiotic stress resistance
journal, August 2013

  • Khan, Abdul Latif; Hussain, Javid; Al-Harrasi, Ahmed
  • Critical Reviews in Biotechnology, Vol. 35, Issue 1
  • DOI: 10.3109/07388551.2013.800018

Drought degree constrains the beneficial effects of a fungal endophyte on Atractylodes lancea
journal, August 2014

  • Yang, T.; Ma, S.; Dai, C. C.
  • Journal of Applied Microbiology, Vol. 117, Issue 5
  • DOI: 10.1111/jam.12615

Ozone and/or Water Stresses Could have Influenced the Betula ermanii Cham. Forest Decline Observed at Oku-Nikko, Japan
journal, December 2006

  • Shimizu, Hideyuki; Feng, Yan Wen
  • Environmental Monitoring and Assessment, Vol. 128, Issue 1-3
  • DOI: 10.1007/s10661-006-9409-0

Climatic response of Betula ermanii along an altitudinal gradient in the northern slope of Changbai Mountain, China
journal, June 2013


Symptomless infection of banana and maize by endophytic fungi impairs photosynthetic efficiency: RESEARCH Endophyte infection and plant metabolism
journal, September 2000


Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi
journal, March 2012

  • Schoch, C. L.; Seifert, K. A.; Huhndorf, S.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 16
  • DOI: 10.1073/pnas.1117018109

Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape
journal, July 2012

  • Zimmerman, N. B.; Vitousek, P. M.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 32
  • DOI: 10.1073/pnas.1209872109

454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases
journal, July 2010


Geographic locality and host identity shape fungal endophyte communities in cupressaceous trees
journal, March 2008


A Hump-Backed Trend in Bacterial Diversity with Elevation on Mount Fuji, Japan
journal, July 2011


Dendroclimatic analysis of Betula ermanii forests at their upper limit of distribution in Changbai Mountain, Northeast China
journal, March 2007


Island species-energy theory
journal, January 2006


Integration of biological networks and gene expression data using Cytoscape
journal, September 2007

  • Cline, Melissa S.; Smoot, Michael; Cerami, Ethan
  • Nature Protocols, Vol. 2, Issue 10
  • DOI: 10.1038/nprot.2007.324

Microbial community resemblance methods differ in their ability to detect biologically relevant patterns
journal, September 2010

  • Kuczynski, Justin; Liu, Zongzhi; Lozupone, Catherine
  • Nature Methods, Vol. 7, Issue 10
  • DOI: 10.1038/nmeth.1499

Metabarcoding Analysis of Fungal Diversity in the Phyllosphere and Carposphere of Olive (Olea europaea)
journal, July 2015


Microbes do not follow the elevational diversity patterns of plants and animals
journal, April 2011

  • Fierer, Noah; McCain, Christy M.; Meir, Patrick
  • Ecology, Vol. 92, Issue 4
  • DOI: 10.1890/10-1170.1

A community of unknown, endophytic fungi in western white pine
journal, June 2004

  • Ganley, R. J.; Brunsfeld, S. J.; Newcombe, G.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 27
  • DOI: 10.1073/pnas.0401513101

Endophytic fungi associated with leaves of Betulaceae in Japan
journal, April 2012

  • Osono, Takashi; Masuya, Hayato
  • Canadian Journal of Microbiology, Vol. 58, Issue 4
  • DOI: 10.1139/w2012-018

Rich and cold: diversity, distribution and drivers of fungal communities in patterned-ground ecosystems of the North American Arctic
journal, April 2014

  • Timling, I.; Walker, D. A.; Nusbaum, C.
  • Molecular Ecology, Vol. 23, Issue 13
  • DOI: 10.1111/mec.12743

Forest vegetation responses to climate and environmental change: A case study from Changbai Mountain, NE China
journal, December 2011


Culture-based study of endophytes associated with rubber trees in Peru reveals a new class of Pezizomycotina: Xylonomycetes
journal, October 2012


The mid-domain effect in ectomycorrhizal fungi: range overlap along an elevation gradient on Mount Fuji, Japan
journal, March 2014

  • Miyamoto, Yumiko; Nakano, Takashi; Hattori, Masahira
  • The ISME Journal, Vol. 8, Issue 8
  • DOI: 10.1038/ismej.2014.34