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Title: Genomic features of bacterial adaptation to plants

Abstract

Plants intimately associate with diverse bacteria. Plant-associated bacteria have ostensibly evolved genes that enable them to adapt to plant environments. However, the identities of such genes are mostly unknown, and their functions are poorly characterized. In this study, we sequenced 484 genomes of bacterial isolates from roots of Brassicaceae, poplar, and maize. We then compared 3,837 bacterial genomes to identify thousands of plant-associated gene clusters. Genomes of plant-associated bacteria encode more carbohydrate metabolism functions and fewer mobile elements than related non-plant-associated genomes do. We experimentally validated candidates from two sets of plant-associated genes: one involved in plant colonization, and the other serving in microbe–microbe competition between plant-associated bacteria. We also identified 64 plant-associated protein domains that potentially mimic plant domains; some are shared with plant-associated fungi and oomycetes. In conclusion, this work expands the genome-based understanding of plant–microbe interactions and provides potential leads for efficient and sustainable agriculture through microbiome engineering.

Authors:
ORCiD logo [1];  [2];  [3]; ORCiD logo [1]; ORCiD logo [4];  [5];  [6];  [7];  [1];  [2];  [1];  [2];  [8];  [9];  [10];  [2];  [2];  [11];  [1]; ORCiD logo [12] more »; ORCiD logo [13]; ORCiD logo [14];  [6];  [7]; ORCiD logo [8];  [3]; ORCiD logo [15]; ORCiD logo [15]; ORCiD logo [16] « less
  1. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  2. Univ. of North Carolina, Chapel Hill, NC (United States). Department of Biology; Howard Hughes Medical Institute, Chevy Chase, MD (United States)
  3. Institute of Microbiology, ETH Zurich (Switzerland)
  4. Univ. of North Carolina, Chapel Hill, NC (United States). Department of Biology; Howard Hughes Medical Institute, Chevy Chase, MD (United States); Stanford Univ., CA (United States). Department of Biology
  5. Virginia Tech, Blacksburg, VA (United States). Department of Horticulture; Gansu Agricultural University (China). The Grassland College
  6. Virginia Tech, Blacksburg, VA (United States). Department of Horticulture
  7. International Centre for Genetic Engineering and Biotechnology, Trieste (Italy)
  8. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
  9. Univ. of Tennessee, Knoxville, TN (United States). Department of Microbiology
  10. Cornell Univ., Ithaca, NY (United States). Department of Molecular Biology and Genetics
  11. Univ. of North Carolina, Chapel Hill, NC (United States). Department of Biology; Howard Hughes Medical Institute, Chevy Chase, MD (United States); BD Technologies and Innovation, Research Triangle Park, NC (United States)
  12. Univ. of North Carolina, Chapel Hill, NC (United States). Department of Biology
  13. Univ. of Washington, Seattle, WA (United States). School of Environmental and Forest Sciences
  14. Max Planck Institute for Developmental Biology, Tubingen (Germany)
  15. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); University of California, Merced, CA (United States)
  16. Univ. of North Carolina, Chapel Hill, NC (United States). Department of Biology, The Carolina Center for Genome Sciences and Department of Microbiology and Immunology; Howard Hughes Medical Institute, Chevy Chase, MD (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23), Biological Systems Science Division (SC-23.2 )
OSTI Identifier:
1415202
Alternate Identifier(s):
OSTI ID: 1529504; OSTI ID: 1571092
Grant/Contract Number:  
AC05-00OR22725; AC02-05CH11231; SC0010423; SC0014395
Resource Type:
Accepted Manuscript
Journal Name:
Nature Genetics
Additional Journal Information:
Journal Volume: 50; Journal Issue: 1; Journal ID: ISSN 1061-4036
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Levy, Asaf, Salas Gonzalez, Isai, Mittelviefhaus, Maximilian, Clingenpeel, Scott, Herrera Paredes, Sur, Miao, Jiamin, Wang, Kunru, Devescovi, Giulia, Stillman, Kyra, Monteiro, Freddy, Rangel Alvarez, Bryan, Lundberg, Derek S., Lu, Tse-Yuan, Lebeis, Sarah, Jin, Zhao, McDonald, Meredith, Klein, Andrew P., Feltcher, Meghan E., Rio, Tijana Glavina, Grant, Sarah R., Doty, Sharon L., Ley, Ruth E., Zhao, Bingyu, Venturi, Vittorio, Pelletier, Dale A., Vorholt, Julia A., Tringe, Susannah G., Woyke, Tanja, and Dangl, Jeffery L. Genomic features of bacterial adaptation to plants. United States: N. p., 2017. Web. doi:10.1038/s41588-017-0012-9.
Levy, Asaf, Salas Gonzalez, Isai, Mittelviefhaus, Maximilian, Clingenpeel, Scott, Herrera Paredes, Sur, Miao, Jiamin, Wang, Kunru, Devescovi, Giulia, Stillman, Kyra, Monteiro, Freddy, Rangel Alvarez, Bryan, Lundberg, Derek S., Lu, Tse-Yuan, Lebeis, Sarah, Jin, Zhao, McDonald, Meredith, Klein, Andrew P., Feltcher, Meghan E., Rio, Tijana Glavina, Grant, Sarah R., Doty, Sharon L., Ley, Ruth E., Zhao, Bingyu, Venturi, Vittorio, Pelletier, Dale A., Vorholt, Julia A., Tringe, Susannah G., Woyke, Tanja, & Dangl, Jeffery L. Genomic features of bacterial adaptation to plants. United States. doi:10.1038/s41588-017-0012-9.
Levy, Asaf, Salas Gonzalez, Isai, Mittelviefhaus, Maximilian, Clingenpeel, Scott, Herrera Paredes, Sur, Miao, Jiamin, Wang, Kunru, Devescovi, Giulia, Stillman, Kyra, Monteiro, Freddy, Rangel Alvarez, Bryan, Lundberg, Derek S., Lu, Tse-Yuan, Lebeis, Sarah, Jin, Zhao, McDonald, Meredith, Klein, Andrew P., Feltcher, Meghan E., Rio, Tijana Glavina, Grant, Sarah R., Doty, Sharon L., Ley, Ruth E., Zhao, Bingyu, Venturi, Vittorio, Pelletier, Dale A., Vorholt, Julia A., Tringe, Susannah G., Woyke, Tanja, and Dangl, Jeffery L. Mon . "Genomic features of bacterial adaptation to plants". United States. doi:10.1038/s41588-017-0012-9. https://www.osti.gov/servlets/purl/1415202.
@article{osti_1415202,
title = {Genomic features of bacterial adaptation to plants},
author = {Levy, Asaf and Salas Gonzalez, Isai and Mittelviefhaus, Maximilian and Clingenpeel, Scott and Herrera Paredes, Sur and Miao, Jiamin and Wang, Kunru and Devescovi, Giulia and Stillman, Kyra and Monteiro, Freddy and Rangel Alvarez, Bryan and Lundberg, Derek S. and Lu, Tse-Yuan and Lebeis, Sarah and Jin, Zhao and McDonald, Meredith and Klein, Andrew P. and Feltcher, Meghan E. and Rio, Tijana Glavina and Grant, Sarah R. and Doty, Sharon L. and Ley, Ruth E. and Zhao, Bingyu and Venturi, Vittorio and Pelletier, Dale A. and Vorholt, Julia A. and Tringe, Susannah G. and Woyke, Tanja and Dangl, Jeffery L.},
abstractNote = {Plants intimately associate with diverse bacteria. Plant-associated bacteria have ostensibly evolved genes that enable them to adapt to plant environments. However, the identities of such genes are mostly unknown, and their functions are poorly characterized. In this study, we sequenced 484 genomes of bacterial isolates from roots of Brassicaceae, poplar, and maize. We then compared 3,837 bacterial genomes to identify thousands of plant-associated gene clusters. Genomes of plant-associated bacteria encode more carbohydrate metabolism functions and fewer mobile elements than related non-plant-associated genomes do. We experimentally validated candidates from two sets of plant-associated genes: one involved in plant colonization, and the other serving in microbe–microbe competition between plant-associated bacteria. We also identified 64 plant-associated protein domains that potentially mimic plant domains; some are shared with plant-associated fungi and oomycetes. In conclusion, this work expands the genome-based understanding of plant–microbe interactions and provides potential leads for efficient and sustainable agriculture through microbiome engineering.},
doi = {10.1038/s41588-017-0012-9},
journal = {Nature Genetics},
number = 1,
volume = 50,
place = {United States},
year = {2017},
month = {12}
}

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Cited by: 20 works
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Figures / Tables:

Figure 1 Figure 1: a. Maximum likelihood phylogenetic tree of 3837 high quality and nonredundant bacterial genomes based on the concatenated alignment of 31 single copy genes. Outer ring denotes the taxonomic group, middle ring denotes the isolation source, and inner ring denotes the RA genomes within PA genomes. Taxon names aremore » color-coded based on phylum: green – Proteobacteria, red – Firmicutes, blue – Bacteroidetes, purple - Actinobacteria. b. Differences in gene categories between PA/NPA and RA/soil genomes of the same taxon. Top panel: PA vs. NPA genomes. Bottom panel: RA vs. soil genomes. For both panels, the heat map indicates the level of enrichment or depletion based on a PhyloGLM test. Significant (colored) cells have p value < 0.05, FDR corrected. Hot colored cells indicate significantly more genes in PA and RA genomes in the upper and lower panels, respectively. Histograms on the upper and right margins represent the total number of genes compared in each column and row, respectively. PA – plant-associated, NPA – non-plant associated, RA – root associated, soil –soil-associated. * not a formal class name. Carbohydrates – Carbohydrate metabolism and transport gene category. Full COG category names from the x axis appear in Table S6. Note that cells with high estimate absolute values (dark colors) are based on categories of few genes and are therefore more likely to be less accurate.« less

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