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Title: Bacterial endophyte communities in Pinus flexilis are structured by host age, tissue type, and environmental factors

Abstract

Background and aims: Forest tree microbiomes are vital to forest dynamics, diversity, and ecosystem processes. Mature limber pines ( Pinus flexilis) host a core microbiome of acetic acid bacteria in their foliage, but the bacterial endophyte community structure, variation, and assembly across tree ontogeny is unknown. The aims of this research were to test if the core microbiome observed in adult P. flexilis is established at the seedling stage, if seedlings host different endophyte communities in root and shoot tissues, and how environmental factors structure seedling endophyte communities. Methods: The 16S rRNA gene was sequenced to characterize the bacterial endophyte communities in roots and shoots of P. flexilis seedlings grown in plots at three elevations at Niwot Ridge, Colorado, subjected to experimental treatments (watering and heating). The data was compared to previously sequenced endophyte communities from adult tree foliage sampled in the same year and location. Results: Seedling shoots hosted a different core microbiome than adult tree foliage and were dominated by a few OTUs in the family Oxalobacteraceae, identical or closely related to strains with antifungal activity. Shoot and root communities significantly differed from each other but shared major OTUs. Watering but not warming restructured the seedling endophyte communities.more » Conclusions: The results indicate differences in assembly and ecological function across conifer life stages. Seedlings may recruit endophytes to protect against fungi under increased soil moisture.« less

Authors:
 [1];  [2];  [3];  [1]
  1. Univ. of California Merced, CA (United States)
  2. Univ. of California Merced, CA (United States); Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. Univ. of California Merced, CA (United States); Univ. of California, Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Science Foundation (NSF); National Institutes of Health (NIH)
OSTI Identifier:
1567127
Grant/Contract Number:  
[AC02-05CH11231]
Resource Type:
Accepted Manuscript
Journal Name:
Plant and Soil
Additional Journal Information:
[ Journal Volume: 428; Journal Issue: 1-2]; Journal ID: ISSN 0032-079X
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 16S rRNA; Endophytic bacteria; Pinus flexilis; Climate change; Conifers

Citation Formats

Carper, Dana L., Carrell, Alyssa A., Kueppers, Lara M., and Frank, A. Carolin. Bacterial endophyte communities in Pinus flexilis are structured by host age, tissue type, and environmental factors. United States: N. p., 2018. Web. doi:10.1007/s11104-018-3682-x.
Carper, Dana L., Carrell, Alyssa A., Kueppers, Lara M., & Frank, A. Carolin. Bacterial endophyte communities in Pinus flexilis are structured by host age, tissue type, and environmental factors. United States. doi:10.1007/s11104-018-3682-x.
Carper, Dana L., Carrell, Alyssa A., Kueppers, Lara M., and Frank, A. Carolin. Wed . "Bacterial endophyte communities in Pinus flexilis are structured by host age, tissue type, and environmental factors". United States. doi:10.1007/s11104-018-3682-x. https://www.osti.gov/servlets/purl/1567127.
@article{osti_1567127,
title = {Bacterial endophyte communities in Pinus flexilis are structured by host age, tissue type, and environmental factors},
author = {Carper, Dana L. and Carrell, Alyssa A. and Kueppers, Lara M. and Frank, A. Carolin},
abstractNote = {Background and aims: Forest tree microbiomes are vital to forest dynamics, diversity, and ecosystem processes. Mature limber pines (Pinus flexilis) host a core microbiome of acetic acid bacteria in their foliage, but the bacterial endophyte community structure, variation, and assembly across tree ontogeny is unknown. The aims of this research were to test if the core microbiome observed in adult P. flexilis is established at the seedling stage, if seedlings host different endophyte communities in root and shoot tissues, and how environmental factors structure seedling endophyte communities. Methods: The 16S rRNA gene was sequenced to characterize the bacterial endophyte communities in roots and shoots of P. flexilis seedlings grown in plots at three elevations at Niwot Ridge, Colorado, subjected to experimental treatments (watering and heating). The data was compared to previously sequenced endophyte communities from adult tree foliage sampled in the same year and location. Results: Seedling shoots hosted a different core microbiome than adult tree foliage and were dominated by a few OTUs in the family Oxalobacteraceae, identical or closely related to strains with antifungal activity. Shoot and root communities significantly differed from each other but shared major OTUs. Watering but not warming restructured the seedling endophyte communities. Conclusions: The results indicate differences in assembly and ecological function across conifer life stages. Seedlings may recruit endophytes to protect against fungi under increased soil moisture.},
doi = {10.1007/s11104-018-3682-x},
journal = {Plant and Soil},
number = [1-2],
volume = [428],
place = {United States},
year = {2018},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Figures / Tables:

Figure 1 Figure 1: Principal coordinate analysis showing differentiation between tissue age, shoot and root communities. (a) unweighted and (b) weighted UniFrac distance matrix. Points that are closer together have more similar communities. Each point corresponds to a sample with the tissue type of each sample indicated by color (blue = shoots/needles,more » green = root) and tissue age indicated by shape (circle = adult, triangle = seedling)« less

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    Works referencing / citing this record:

    N2-Fixation and Seedling Growth Promotion of Lodgepole Pine by Endophytic Paenibacillus polymyxa
    journal, February 2013


    The Diversity of Archaea and Bacteria in Association with the Roots of Zea mays L.
    journal, February 2001


    Warming and the dependence of limber pine (Pinus flexilis) establishment on summer soil moisture within and above its current elevation range
    journal, August 2012


    Biodiversity and physiological characteristics of Antarctic and Arctic lichens-associated bacteria
    journal, July 2014

    • Lee, Yung Mi; Kim, Eun Hye; Lee, Hong Kum
    • World Journal of Microbiology and Biotechnology, Vol. 30, Issue 10
    • DOI: 10.1007/s11274-014-1695-z

    Isolation and phylogenetic classification of culturable psychrophilic prokaryotes from the Collins glacier in the Antarctica
    journal, May 2011

    • García-Echauri, S. A.; Gidekel, M.; Gutiérrez-Moraga, A.
    • Folia Microbiologica, Vol. 56, Issue 3
    • DOI: 10.1007/s12223-011-0038-9

    Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17
    journal, January 2014


    A comparison of the community diversity of foliar fungal endophytes between seedling and adult loblolly pines ( Pinus taeda )
    journal, October 2015


    Foliar nutrients shape fungal endophyte communities in Western white pine (Pinus monticola) with implications for white-tailed deer herbivory
    journal, April 2012


    Dissecting endophytic lifestyle along the parasitism/mutualism continuum in Arabidopsis
    journal, August 2016


    Experimental warming effects on the microbial community of a temperate mountain forest soil
    journal, July 2011


    Contrasting patterns of seed and root colonization by bacteria from the genus Chryseobacterium and from the family Oxalobacteraceae
    journal, May 2007

    • Green, Stefan J.; Michel, Frederick C.; Hadar, Yitzhak
    • The ISME Journal, Vol. 1, Issue 4
    • DOI: 10.1038/ismej.2007.33

    Defining the core Arabidopsis thaliana root microbiome
    journal, August 2012

    • Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera
    • Nature, Vol. 488, Issue 7409
    • DOI: 10.1038/nature11237

    Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota
    journal, August 2012

    • Bulgarelli, Davide; Rott, Matthias; Schlaeppi, Klaus
    • Nature, Vol. 488, Issue 7409
    • DOI: 10.1038/nature11336

    Root microbiota drive direct integration of phosphate stress and immunity
    journal, March 2017

    • Castrillo, Gabriel; Teixeira, Paulo José Pereira Lima; Paredes, Sur Herrera
    • Nature, Vol. 543, Issue 7646
    • DOI: 10.1038/nature21417

    Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing
    journal, December 2012

    • Bokulich, Nicholas A.; Subramanian, Sathish; Faith, Jeremiah J.
    • Nature Methods, Vol. 10, Issue 1
    • DOI: 10.1038/nmeth.2276

    Differential abundance analysis for microbial marker-gene surveys
    journal, September 2013

    • Paulson, Joseph N.; Stine, O. Colin; Bravo, Héctor Corrada
    • Nature Methods, Vol. 10, Issue 12
    • DOI: 10.1038/nmeth.2658

    Evolutionary conservation of a core root microbiome across plant phyla along a tropical soil chronosequence
    journal, August 2017

    • Yeoh, Yun Kit; Dennis, Paul G.; Paungfoo-Lonhienne, Chanyarat
    • Nature Communications, Vol. 8, Issue 1
    • DOI: 10.1038/s41467-017-00262-8

    Cellulose and hemicellulose decomposition by forest soil bacteria proceeds by the action of structurally variable enzymatic systems
    journal, April 2016

    • López-Mondéjar, Rubén; Zühlke, Daniela; Becher, Dörte
    • Scientific Reports, Vol. 6, Issue 1
    • DOI: 10.1038/srep25279

    Sky exposure, crown architecture, and low-temperature photoinhibition in conifer seedlings at alpine treeline
    journal, April 1999


    Microbiome of the upper troposphere: Species composition and prevalence, effects of tropical storms, and atmospheric implications
    journal, January 2013

    • DeLeon-Rodriguez, N.; Lathem, T. L.; Rodriguez-R, L. M.
    • Proceedings of the National Academy of Sciences, Vol. 110, Issue 7
    • DOI: 10.1073/pnas.1212089110

    Diversity and heritability of the maize rhizosphere microbiome under field conditions
    journal, April 2013

    • Peiffer, J. A.; Spor, A.; Koren, O.
    • Proceedings of the National Academy of Sciences, Vol. 110, Issue 16
    • DOI: 10.1073/pnas.1302837110

    Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives
    journal, December 2013

    • Schlaeppi, K.; Dombrowski, N.; Oter, R. G.
    • Proceedings of the National Academy of Sciences, Vol. 111, Issue 2
    • DOI: 10.1073/pnas.1321597111

    Structure, variation, and assembly of the root-associated microbiomes of rice
    journal, January 2015

    • Edwards, Joseph; Johnson, Cameron; Santos-Medellín, Christian
    • Proceedings of the National Academy of Sciences, Vol. 112, Issue 8
    • DOI: 10.1073/pnas.1414592112

    Deciduous forest responses to temperature, precipitation, and drought imply complex climate change impacts
    journal, October 2015

    • Xie, Yingying; Wang, Xiaojing; Silander, John A.
    • Proceedings of the National Academy of Sciences, Vol. 112, Issue 44
    • DOI: 10.1073/pnas.1509991112

    Isolation and Characterization of Rumex acetosa -Associated Mineral-Weathering Bacteria
    journal, July 2017


    Forest pathogens with higher damage potential due to climate change in Europe
    journal, April 2008


    Conifer seedling recruitment across a gradient from forest to alpine tundra: effects of species, provenance, and site
    journal, December 2013


    PyNAST: a flexible tool for aligning sequences to a template alignment
    journal, November 2009


    Census of bacterial microbiota associated with the glacier ice worm Mesenchytraeus solifugus
    journal, January 2015

    • Murakami, Takumi; Segawa, Takahiro; Bodington, Dylan
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    • DOI: 10.1093/femsec/fiv003

    Subalpine conifers in different geographical locations host highly similar foliar bacterial endophyte communities
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    • Carrell, Alyssa A.; Carper, Dana L.; Frank, A. Carolin
    • FEMS Microbiology Ecology, Vol. 92, Issue 8
    • DOI: 10.1093/femsec/fiw124

    Interactive effects of water and nitrogen addition on soil microbial communities in a semiarid steppe
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    FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix
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    • DOI: 10.1093/molbev/msp077

    SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB
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    Another perspective on altitudinal limits of alpine timberlines
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    Ecophysiological variation in two provenances of Pinus flexilis seedlings across an elevation gradient from forest to alpine
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    • Reinhardt, Keith; Castanha, Cristina; Germino, Matthew J.
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    Probiotic treatment restores protection against lethal fungal infection lost during amphibian captivity
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    • DOI: 10.1098/rspb.2016.1553

    Sphingomonas psychrolutea sp. nov., a psychrotolerant bacterium isolated from glacier ice
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    • Zhou, Yu-Guang; Liu, Qing; Zhang, Jian-Li
    • International Journal of Systematic and Evolutionary Microbiology, Vol. 65, Issue 9
    • DOI: 10.1099/ijs.0.000362

    Mucilaginibacter pineti sp. nov., isolated from Pinus pinaster wood from a mixed grove of pines trees
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    • DOI: 10.1099/ijs.0.057737-0

    Warming and provenance limit tree recruitment across and beyond the elevation range of subalpine forest
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    • Kueppers, Lara M.; Conlisk, Erin; Castanha, Cristina
    • Global Change Biology, Vol. 23, Issue 6
    • DOI: 10.1111/gcb.13561

    Enrichment for microbes living in association with plant tissues
    journal, April 2006


    The bacterial genus Collimonas : mycophagy, weathering and other adaptive solutions to life in oligotrophic soil environments
    journal, February 2010


    Wood-decay fungi in fine living roots of conifer seedlings
    journal, April 2007


    Fungal endophytes: diversity and functional roles
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    Potential for atmospheric deposition of bacteria to influence bacterioplankton communities: Atmospheric deposition as immigration events
    journal, April 2008


    Endophytic bacterial communities in three arctic plants from low arctic fell tundra are cold-adapted and host-plant specific
    journal, August 2012


    Bacterial diversity in the rhizosphere of maize and the surrounding carbonate-rich bulk soil: Biodiversity in adjacent niches
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    Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants
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    • DOI: 10.1111/mec.12821

    Evidence for foliar endophytic nitrogen fixation in a widely distributed subalpine conifer
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    • DOI: 10.1111/nph.13850

    Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa
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    Composition and variation of the skin microbiota in sympatric species of European newts (Salamandridae)
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    Interactive metagenomic visualization in a Web browser
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    Ecology of Root Colonizing Massilia (Oxalobacteraceae)
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    A Drought Resistance-Promoting Microbiome Is Selected by Root System under Desert Farming
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    Bacterial Communities Associated with the Leaves and the Roots of Arabidopsis thaliana
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    phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
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    A Multifactor Analysis of Fungal and Bacterial Community Structure in the Root Microbiome of Mature Populus deltoides Trees
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    Soil Bacterial Communities Respond to Climate Changes in a Temperate Steppe
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    Long-term forest soil warming alters microbial communities in temperate forest soils
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    Seasonal variation of bacterial endophytes in urban trees
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    Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates
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    Bacterial endophyte communities in the foliage of coast redwood and giant sequoia
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    Molecular Keys to the Janthinobacterium and Duganella spp. Interaction with the Plant Pathogen Fusarium graminearum
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    A Phloem-Feeding Insect Transfers Bacterial Endophytic Communities between Grapevine Plants
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    Mechanisms of plant defense against insect herbivores
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    Data from: The unique ecology of human predators
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    Endophytic bacterial community living in roots of healthy and ‘Candidatus Phytoplasma mali’-infected apple (Malus domestica, Borkh.) trees
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    UPARSE: highly accurate OTU sequences from microbial amplicon reads
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    Soil microbial and nutrient responses to 7 years of seasonally altered precipitation in a Chihuahuan Desert grassland
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    Interactions with soil biota shift from negative to positive when a tree species is moved outside its native range
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    Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species
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    Isolation and identification of diazotrophic bacteria from internal tissues of Pinus contorta and Thuja plicata
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      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.