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Title: Niche differentiation is spatially and temporally regulated in the rhizosphere

Abstract

The rhizosphere is a hotspot for microbial carbon transformations, and is the entry point for root polysaccharides and polymeric carbohydrates that are important precursors to soil organic matter (SOM). However, the ecological mechanisms that underpin rhizosphere carbohydrate depolymerization are poorly understood. Using Avena fatua, a common annual grass, we analyzed time-resolved metatranscriptomes to compare microbial functions in rhizosphere, detritusphere, and combined rhizosphere-detritusphere habitats. Transcripts were binned using a unique reference database generated from soil isolate genomes, single-cell amplified genomes, metagenomes, and stable isotope probing metagenomes. While soil habitat significantly affected both community composition and overall gene expression, the succession of microbial functions occurred at a faster time scale than compositional changes. Using hierarchical clustering of upregulated decomposition genes, we identified four distinct microbial guilds populated by taxa whose functional succession patterns suggest specialization for substrates provided by fresh growing roots, decaying root detritus, the combination of live and decaying root biomass, or aging root material. Carbohydrate depolymerization genes were consistently upregulated in the rhizosphere, and both taxonomic and functional diversity were highest in the combined rhizosphere-detritusphere, suggesting coexistence of rhizosphere guilds is facilitated by niche differentiation. Finally, metatranscriptome-defined guilds provide a framework to model rhizosphere succession and its consequences formore » soil carbon cycling.« less

Authors:
ORCiD logo [1];  [2]; ORCiD logo [3]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [5];  [5]; ORCiD logo [5]; ORCiD logo [6];  [6]; ORCiD logo [1]
  1. Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
  2. Univ. of California, Berkeley, CA (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of Oklahoma, Norman, OK (United States); Tsinghua Univ., Beijing (China)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. Lawrence Berkeley National Lab. (LBNL), Berkeley, 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)
OSTI Identifier:
1597728
Grant/Contract Number:  
[AC02-05CH11231; SCW1589; SCW1039; SC0010570; SC0016247; SC10010566; AC52-07NA27344]
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
[Journal Name: The ISME Journal]; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
microbial ecology; microbiome; soil microbiology

Citation Formats

Nuccio, Erin E., Starr, Evan, Karaoz, Ulas, Brodie, Eoin L., Zhou, Jizhong, Tringe, Susannah G., Malmstrom, Rex R., Woyke, Tanja, Banfield, Jillian F., Firestone, Mary K., and Pett-Ridge, Jennifer. Niche differentiation is spatially and temporally regulated in the rhizosphere. United States: N. p., 2020. Web. doi:10.1038/s41396-019-0582-x.
Nuccio, Erin E., Starr, Evan, Karaoz, Ulas, Brodie, Eoin L., Zhou, Jizhong, Tringe, Susannah G., Malmstrom, Rex R., Woyke, Tanja, Banfield, Jillian F., Firestone, Mary K., & Pett-Ridge, Jennifer. Niche differentiation is spatially and temporally regulated in the rhizosphere. United States. doi:10.1038/s41396-019-0582-x.
Nuccio, Erin E., Starr, Evan, Karaoz, Ulas, Brodie, Eoin L., Zhou, Jizhong, Tringe, Susannah G., Malmstrom, Rex R., Woyke, Tanja, Banfield, Jillian F., Firestone, Mary K., and Pett-Ridge, Jennifer. Fri . "Niche differentiation is spatially and temporally regulated in the rhizosphere". United States. doi:10.1038/s41396-019-0582-x.
@article{osti_1597728,
title = {Niche differentiation is spatially and temporally regulated in the rhizosphere},
author = {Nuccio, Erin E. and Starr, Evan and Karaoz, Ulas and Brodie, Eoin L. and Zhou, Jizhong and Tringe, Susannah G. and Malmstrom, Rex R. and Woyke, Tanja and Banfield, Jillian F. and Firestone, Mary K. and Pett-Ridge, Jennifer},
abstractNote = {The rhizosphere is a hotspot for microbial carbon transformations, and is the entry point for root polysaccharides and polymeric carbohydrates that are important precursors to soil organic matter (SOM). However, the ecological mechanisms that underpin rhizosphere carbohydrate depolymerization are poorly understood. Using Avena fatua, a common annual grass, we analyzed time-resolved metatranscriptomes to compare microbial functions in rhizosphere, detritusphere, and combined rhizosphere-detritusphere habitats. Transcripts were binned using a unique reference database generated from soil isolate genomes, single-cell amplified genomes, metagenomes, and stable isotope probing metagenomes. While soil habitat significantly affected both community composition and overall gene expression, the succession of microbial functions occurred at a faster time scale than compositional changes. Using hierarchical clustering of upregulated decomposition genes, we identified four distinct microbial guilds populated by taxa whose functional succession patterns suggest specialization for substrates provided by fresh growing roots, decaying root detritus, the combination of live and decaying root biomass, or aging root material. Carbohydrate depolymerization genes were consistently upregulated in the rhizosphere, and both taxonomic and functional diversity were highest in the combined rhizosphere-detritusphere, suggesting coexistence of rhizosphere guilds is facilitated by niche differentiation. Finally, metatranscriptome-defined guilds provide a framework to model rhizosphere succession and its consequences for soil carbon cycling.},
doi = {10.1038/s41396-019-0582-x},
journal = {The ISME Journal},
number = ,
volume = ,
place = {United States},
year = {2020},
month = {1}
}

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