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Title: Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism

Abstract

The circadian clock regulates plant metabolic functions and is an important component in plant health and productivity. Rhizosphere bacteria play critical roles in plant growth, health, and development and are shaped primarily by soil communities. Using Illumina next-generation sequencing and high-resolution mass spectrometry, we characterized bacterial communities of wild-type (Col-0) Arabidopsis thaliana and an acyclic line (OX34) ectopically expressing the circadian clock-associated cca1 transcription factor, relative to a soil control, to determine how cycling dynamics affected the microbial community. Microbial communities associated with Brachypodium distachyon (BD21) were also evaluated.Significantly different bacterial community structures ( P = 0.031) were observed in the rhizosphere of wild-type plants between light and dark cycle samples. Furthermore, 13% of the community showed cycling, with abundances of several families, including Burkholderiaceae, Rhodospirillaceae, Planctomycetaceae, and Gaiellaceae, exhibiting fluctuation in abundances relative to the light cycle. However, limited-to-no cycling was observed in the acyclic CCAox34 line or in soil controls. Significant cycling was also observed, to a lesser extent, in Brachypodium. Functional gene inference revealed that genes involved in carbohydrate metabolism were likely more abundant in near-dawn, dark samples. Additionally, the composition of organic matter in the rhizosphere showed a significant variation between dark and light cycles.The resultsmore » of this study suggest that the rhizosphere bacterial community is regulated, to some extent, by the circadian clock and is likely influenced by, and exerts influences, on plant metabolism and productivity. The timing of bacterial cycling in relation to that of Arabidopsis further suggests that diurnal dynamics influence plant-microbe carbon metabolism and exchange. Equally important, our results suggest that previous studies done without relevance to time of day may need to be reevaluated with regard to the impact of diurnal cycles on the rhizosphere microbial community.« less

Authors:
 [1];  [2];  [2];  [3];  [2];  [1];  [2];  [2];  [2];  [2];  [2];  [3];  [3];  [3];  [3];  [4];  [5];  [2];  [3];  [1]
  1. Univ. of Minnesota, St. Paul, MN (United States)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  3. Univ. of Missouri, Columbia, MO (United States)
  4. Univ. of Missouri Research Reactor, Columbia, MO (United States)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1406756
Alternate Identifier(s):
OSTI ID: 1379894
Report Number(s):
PNNL-SA-121718
Journal ID: ISSN 2049-2618; ark:/13030/qt03s3j0xv
Grant/Contract Number:  
AC02-05CH11231; AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Microbiome
Additional Journal Information:
Journal Volume: 5; Journal Issue: 1; Journal ID: ISSN 2049-2618
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Bacterial community structure; Diurnal rhythm; Rhizosphere; Arabidopsis; Environmental Molecular Sciences Laboratory

Citation Formats

Staley, Christopher, Ferrieri, Abigail P., Tfaily, Malak M., Cui, Yaya, Chu, Rosalie K., Wang, Ping, Shaw, Jared B., Ansong, Charles K., Brewer, Heather, Norbeck, Angela D., Markillie, Meng, do Amaral, Fernanda, Tuleski, Thalita, Pellizzaro, Tomas, Agtuca, Beverly, Ferrieri, Richard, Tringe, Susannah G., Pasa-Tolic, Ljiljana, Stacey, Gary, and Sadowsky, Michael J. Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism. United States: N. p., 2017. Web. doi:10.1186/s40168-017-0287-1.
Staley, Christopher, Ferrieri, Abigail P., Tfaily, Malak M., Cui, Yaya, Chu, Rosalie K., Wang, Ping, Shaw, Jared B., Ansong, Charles K., Brewer, Heather, Norbeck, Angela D., Markillie, Meng, do Amaral, Fernanda, Tuleski, Thalita, Pellizzaro, Tomas, Agtuca, Beverly, Ferrieri, Richard, Tringe, Susannah G., Pasa-Tolic, Ljiljana, Stacey, Gary, & Sadowsky, Michael J. Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism. United States. doi:10.1186/s40168-017-0287-1.
Staley, Christopher, Ferrieri, Abigail P., Tfaily, Malak M., Cui, Yaya, Chu, Rosalie K., Wang, Ping, Shaw, Jared B., Ansong, Charles K., Brewer, Heather, Norbeck, Angela D., Markillie, Meng, do Amaral, Fernanda, Tuleski, Thalita, Pellizzaro, Tomas, Agtuca, Beverly, Ferrieri, Richard, Tringe, Susannah G., Pasa-Tolic, Ljiljana, Stacey, Gary, and Sadowsky, Michael J. Sat . "Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism". United States. doi:10.1186/s40168-017-0287-1. https://www.osti.gov/servlets/purl/1406756.
@article{osti_1406756,
title = {Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism},
author = {Staley, Christopher and Ferrieri, Abigail P. and Tfaily, Malak M. and Cui, Yaya and Chu, Rosalie K. and Wang, Ping and Shaw, Jared B. and Ansong, Charles K. and Brewer, Heather and Norbeck, Angela D. and Markillie, Meng and do Amaral, Fernanda and Tuleski, Thalita and Pellizzaro, Tomas and Agtuca, Beverly and Ferrieri, Richard and Tringe, Susannah G. and Pasa-Tolic, Ljiljana and Stacey, Gary and Sadowsky, Michael J.},
abstractNote = {The circadian clock regulates plant metabolic functions and is an important component in plant health and productivity. Rhizosphere bacteria play critical roles in plant growth, health, and development and are shaped primarily by soil communities. Using Illumina next-generation sequencing and high-resolution mass spectrometry, we characterized bacterial communities of wild-type (Col-0) Arabidopsis thaliana and an acyclic line (OX34) ectopically expressing the circadian clock-associated cca1 transcription factor, relative to a soil control, to determine how cycling dynamics affected the microbial community. Microbial communities associated with Brachypodium distachyon (BD21) were also evaluated.Significantly different bacterial community structures (P = 0.031) were observed in the rhizosphere of wild-type plants between light and dark cycle samples. Furthermore, 13% of the community showed cycling, with abundances of several families, including Burkholderiaceae, Rhodospirillaceae, Planctomycetaceae, and Gaiellaceae, exhibiting fluctuation in abundances relative to the light cycle. However, limited-to-no cycling was observed in the acyclic CCAox34 line or in soil controls. Significant cycling was also observed, to a lesser extent, in Brachypodium. Functional gene inference revealed that genes involved in carbohydrate metabolism were likely more abundant in near-dawn, dark samples. Additionally, the composition of organic matter in the rhizosphere showed a significant variation between dark and light cycles.The results of this study suggest that the rhizosphere bacterial community is regulated, to some extent, by the circadian clock and is likely influenced by, and exerts influences, on plant metabolism and productivity. The timing of bacterial cycling in relation to that of Arabidopsis further suggests that diurnal dynamics influence plant-microbe carbon metabolism and exchange. Equally important, our results suggest that previous studies done without relevance to time of day may need to be reevaluated with regard to the impact of diurnal cycles on the rhizosphere microbial community.},
doi = {10.1186/s40168-017-0287-1},
journal = {Microbiome},
number = 1,
volume = 5,
place = {United States},
year = {2017},
month = {6}
}

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Figures / Tables:

Table 1 Table 1: Coverage and alpha diversity (mean ± standard deviation) among AM and PM rhizosphere samples based on 16S rRNA gene sequencing

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    Works referencing / citing this record:

    Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism [Supplemental Data]
    dataset, June 2017

    • Staley, Christopher; Ferrieri, Abigail; Tfaily, Malak
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