Microbial Interkingdom Interactions in Roots Promote Arabidopsis Survival

被引:681
作者
Duran, Paloma [1 ]
Thiergart, Thorsten [1 ]
Garrido-Oter, Ruben [1 ,2 ]
Agler, Matthew [1 ,3 ]
Kemen, Eric [1 ,2 ,4 ]
Schulze-Lefert, Paul [1 ,2 ]
Hacquard, Stephane [1 ]
机构
[1] Max Planck Inst Plant Breeding Res, D-50829 Cologne, Germany
[2] Max Planck Inst Plant Breeding Res, Cluster Excellence Plant Sci CEPLAS, D-50829 Cologne, Germany
[3] Friedrich Schiller Univ, Inst Microbiol, D-07743 Jena, Germany
[4] Univ Tubingen, IMIT ZMBP, Dept Microbial Interact, D-72076 Tubingen, Germany
基金
欧洲研究理事会;
关键词
BAYESIAN CLASSIFIER; PLANT; FUNGAL; SEQUENCES; CONVERGENCE; NUTRITION; SYMBIOSIS; THALIANA; BACTERIA; TOOL;
D O I
10.1016/j.cell.2018.10.020
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Roots of healthy plants are inhabited by soil-derived bacteria, fungi, and oomycetes that have evolved independently in distinct kingdoms of life. How these microorganisms interact and to what extent those interactions affect plant health are poorly understood. We examined root-associated microbial communities from three Arabidopsis thaliana populations and detected mostly negative correlations between bacteria and filamentous microbial eukaryotes. We established microbial culture collections for reconstitution experiments using germ-free A. thaliana. In plants inoculated with mono- or multi-kingdom synthetic microbial consortia, we observed a profound impact of the bacterial root microbiota on fungal and oomycetal community structure and diversity. We demonstrate that the bacterial microbiota is essential for plant survival and protection against root-derived filamentous eukaryotes. Deconvolution of 2,862 binary bacterial-fungal interactions ex situ, combined with community perturbation experiments in planta, indicate that biocontrol activity of bacterial root commensals is a redundant trait that maintains microbial interkingdom balance for plant health.
引用
收藏
页码:973 / +
页数:25
相关论文
共 41 条
[1]   Microbial Hub Taxa Link Host and Abiotic Factors to Plant Microbiome Variation [J].
Agler, Matthew T. ;
Ruhe, Jonas ;
Kroll, Samuel ;
Morhenn, Constanze ;
Kim, Sang-Tae ;
Weigel, Detlef ;
Kemen, Eric M. .
PLOS BIOLOGY, 2016, 14 (01)
[2]   T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks [J].
Alix, Boc ;
Boubacar, Diallo Alpha ;
Vladimir, Makarenkov .
NUCLEIC ACIDS RESEARCH, 2012, 40 (W1) :W573-W579
[3]   Root-associated fungal microbiota of nonmycorrhizal &ITArabis&IT &ITalpina &ITand its contribution to plant phosphorus nutrition [J].
Almario, Juliana ;
Jeena, Ganga ;
Wunder, Joerg ;
Langen, Gregor ;
Zuccaro, Alga ;
Coupland, George ;
Bucher, Marcel .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2017, 114 (44) :E9403-E9412
[4]   Functional overlap of the Arabidopsis leaf and root microbiota [J].
Bai, Yang ;
Mueller, Daniel B. ;
Srinivas, Girish ;
Garrido-Oter, Ruben ;
Potthoff, Eva ;
Rott, Matthias ;
Dombrowski, Nina ;
Muench, Philipp C. ;
Spaepen, Stijn ;
Remus-Emsermann, Mitja ;
Huettel, Bruno ;
McHardy, Alice C. ;
Vorholt, Julia A. ;
Schulze-Lefert, Paul .
NATURE, 2015, 528 (7582) :364-+
[5]   Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data [J].
Bengtsson-Palme, Johan ;
Ryberg, Martin ;
Hartmann, Martin ;
Branco, Sara ;
Wang, Zheng ;
Godhe, Anna ;
De Wit, Pierre ;
Sanchez-Garcia, Marisol ;
Ebersberger, Ingo ;
de Sousa, Filipe ;
Amend, Anthony S. ;
Jumpponen, Ari ;
Unterseher, Martin ;
Kristiansson, Erik ;
Abarenkov, Kessy ;
Bertrand, Yann J. K. ;
Sanli, Kemal ;
Eriksson, K. Martin ;
Vik, Unni ;
Veldre, Vilmar ;
Nilsson, R. Henrik .
METHODS IN ECOLOGY AND EVOLUTION, 2013, 4 (10) :914-919
[6]   Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota [J].
Bulgarelli, Davide ;
Rott, Matthias ;
Schlaeppi, Klaus ;
van Themaat, Emiel Ver Loren ;
Ahmadinejad, Nahal ;
Assenza, Federica ;
Rauf, Philipp ;
Huettel, Bruno ;
Reinhardt, Richard ;
Schmelzer, Elmon ;
Peplies, Joerg ;
Gloeckner, Frank Oliver ;
Amann, Rudolf ;
Eickhorst, Thilo ;
Schulze-Lefert, Paul .
NATURE, 2012, 488 (7409) :91-95
[7]   QIIME allows analysis of high-throughput community sequencing data [J].
Caporaso, J. Gregory ;
Kuczynski, Justin ;
Stombaugh, Jesse ;
Bittinger, Kyle ;
Bushman, Frederic D. ;
Costello, Elizabeth K. ;
Fierer, Noah ;
Pena, Antonio Gonzalez ;
Goodrich, Julia K. ;
Gordon, Jeffrey I. ;
Huttley, Gavin A. ;
Kelley, Scott T. ;
Knights, Dan ;
Koenig, Jeremy E. ;
Ley, Ruth E. ;
Lozupone, Catherine A. ;
McDonald, Daniel ;
Muegge, Brian D. ;
Pirrung, Meg ;
Reeder, Jens ;
Sevinsky, Joel R. ;
Tumbaugh, Peter J. ;
Walters, William A. ;
Widmann, Jeremy ;
Yatsunenko, Tanya ;
Zaneveld, Jesse ;
Knight, Rob .
NATURE METHODS, 2010, 7 (05) :335-336
[8]   PyNAST: a flexible tool for aligning sequences to a template alignment [J].
Caporaso, J. Gregory ;
Bittinger, Kyle ;
Bushman, Frederic D. ;
DeSantis, Todd Z. ;
Andersen, Gary L. ;
Knight, Rob .
BIOINFORMATICS, 2010, 26 (02) :266-267
[9]   Root microbiota drive direct integration of phosphate stress and immunity [J].
Castrillo, Gabriel ;
Teixeira, Paulo Jose Pereira Lima ;
Paredes, Sur Herrera ;
Law, Theresa F. ;
de Lorenzo, Laura ;
Feltcher, Meghan E. ;
Finkel, Omri M. ;
Breakfield, Natalie W. ;
Mieczkowski, Piotr ;
Jones, Corbin D. ;
Paz-Ares, Javier ;
Dangl, Jeffery L. .
NATURE, 2017, 543 (7646) :513-+
[10]   Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species [J].
Coleman-Derr, Devin ;
Desgarennes, Damaris ;
Fonseca-Garcia, Citlali ;
Gross, Stephen ;
Clingenpeel, Scott ;
Woyke, Tanja ;
North, Gretchen ;
Visel, Axel ;
Partida-Martinez, Laila P. ;
Tringe, Susannah G. .
NEW PHYTOLOGIST, 2016, 209 (02) :798-811