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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 results ofmore » 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:
; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1618946
Alternate Identifier(s):
OSTI ID: 1379894; OSTI ID: 1406756
Report Number(s):
PNNL-SA-121718
Journal ID: ISSN 2049-2618; 65; PII: 287
Grant/Contract Number:  
AC02-05CH11231; AC05-76RL01830; DESC0013978
Resource Type:
Published Article
Journal Name:
Microbiome
Additional Journal Information:
Journal Name: Microbiome Journal Volume: 5 Journal Issue: 1; Journal ID: ISSN 2049-2618
Publisher:
Springer Science + Business Media
Country of Publication:
United Kingdom
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, Tomás, Agtuca, Beverly, Ferrieri, Richard, Tringe, Susannah G., Paša-Tolić, Ljiljana, Stacey, Gary, and Sadowsky, Michael J. Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism. United Kingdom: 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, Tomás, Agtuca, Beverly, Ferrieri, Richard, Tringe, Susannah G., Paša-Tolić, Ljiljana, Stacey, Gary, & Sadowsky, Michael J. Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism. United Kingdom. https://doi.org/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, Tomás, Agtuca, Beverly, Ferrieri, Richard, Tringe, Susannah G., Paša-Tolić, Ljiljana, Stacey, Gary, and Sadowsky, Michael J. Sat . "Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism". United Kingdom. https://doi.org/10.1186/s40168-017-0287-1.
@article{osti_1618946,
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, Tomás and Agtuca, Beverly and Ferrieri, Richard and Tringe, Susannah G. and Paša-Tolić, 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 Kingdom},
year = {Sat Jun 24 00:00:00 EDT 2017},
month = {Sat Jun 24 00:00:00 EDT 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1186/s40168-017-0287-1

Citation Metrics:
Cited by: 36 works
Citation information provided by
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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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