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

Christopher Staley; Abigail P. Ferrieri; Malak M. Tfaily; Yaya Cui; Rosalie K. Chu; Ping Wang; Jared B. Shaw; Charles K. Ansong; Heather Brewer; Angela D. Norbeck; Meng Markillie; Fernanda do Amaral; Thalita Tuleski; Tomás Pellizzaro; Beverly Agtuca; Richard Ferrieri; Susannah G. Tringe; Ljiljana Paša-Tolić; Gary Stacey; Michael J. Sadowsky

doi:10.1186/s40168-017-0287-1

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

Christopher Staley, Abigail P. Ferrieri, Malak M. Tfaily, Yaya Cui, Rosalie K. Chu, Ping Wang, Jared B. Shaw, Charles K. Ansong, Heather Brewer, Angela D. Norbeck, Meng Markillie, Fernanda do Amaral, Thalita Tuleski, Tomás Pellizzaro, Beverly Agtuca, Richard Ferrieri, Susannah G. Tringe, Ljiljana Paša-Tolić, Gary Stacey, Michael J. Sadowsky

Research output: Contribution to journal › Article › peer-review

66 Scopus citations

Abstract

BACKGROUND: 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.

RESULTS: 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.

CONCLUSIONS: 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.

Original language	English (US)
Pages (from-to)	65
Number of pages	1
Journal	Microbiome
Volume	5
Issue number	1
DOIs	https://doi.org/10.1186/s40168-017-0287-1
State	Published - Jun 24 2017
Externally published	Yes

Keywords

Arabidopsis
Bacterial community structure
Diurnal rhythm
Rhizosphere

ASJC Scopus subject areas

Microbiology
Microbiology (medical)

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10.1186/s40168-017-0287-1

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Staley, C., Ferrieri, A. P., Tfaily, M. M., Cui, Y., Chu, R. K., Wang, P., Shaw, J. B., Ansong, C. K., Brewer, H., Norbeck, A. D., Markillie, M., do Amaral, F., Tuleski, T., Pellizzaro, T., Agtuca, B., Ferrieri, R., Tringe, S. G., Paša-Tolić, L., Stacey, G., & Sadowsky, M. J. (2017). Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism. Microbiome, 5(1), 65. https://doi.org/10.1186/s40168-017-0287-1

Staley, C, Ferrieri, AP, Tfaily, MM, Cui, Y, Chu, RK, Wang, P, Shaw, JB, Ansong, CK, Brewer, H, Norbeck, AD, Markillie, M, do Amaral, F, Tuleski, T, Pellizzaro, T, Agtuca, B, Ferrieri, R, Tringe, SG, Paša-Tolić, L, Stacey, G & Sadowsky, MJ 2017, 'Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism', Microbiome, vol. 5, no. 1, pp. 65. https://doi.org/10.1186/s40168-017-0287-1

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title = "Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism",

abstract = "BACKGROUND: 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.RESULTS: 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.CONCLUSIONS: 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.",

keywords = "Arabidopsis, Bacterial community structure, Diurnal rhythm, Rhizosphere",

author = "Christopher Staley and Ferrieri, {Abigail P.} and Tfaily, {Malak M.} and Yaya Cui and Chu, {Rosalie K.} and Ping Wang and Shaw, {Jared B.} and Ansong, {Charles K.} and Heather Brewer and Norbeck, {Angela D.} and Meng Markillie and {do Amaral}, Fernanda and Thalita Tuleski and Tom{\'a}s Pellizzaro and Beverly Agtuca and Richard Ferrieri and Tringe, {Susannah G.} and Ljiljana Pa{\v s}a-Toli{\'c} and Gary Stacey and Sadowsky, {Michael J.}",

note = "Funding Information: The work conducted by the DOE Joint Genome Institute and EMSL is supported by the Office of Science of the DOE under contract no. DE-AC02-05CH11231 (JGI) and DE-AC05-76RL01830 (EMSL). Work was also funded, in part, by a grant from the DOE Office of Science, Biological and Environmental Research (Grant No. DESC0013978 to GS). Funding Information: Special thanks to Dr. Rob McClung (Dartmouth Univ.) for providing seeds of the CCA1ox line. Sequence processing and analysis was performed, in part, using the resources of the Minnesota Supercomputing Institute. Mass spectrometry was performed using the Environmental and Molecular Sciences Laboratory (EMSL), a US Department of Energy (DOE) Office of Science User Facility sponsored by Biological and Environmental Research (BER) and located at Pacific Northwest National Laboratory (PNNL). PNNL is operated by Battelle for DOE.",

year = "2017",

month = jun,

day = "24",

doi = "10.1186/s40168-017-0287-1",

language = "English (US)",

volume = "5",

pages = "65",

journal = "Microbiome",

issn = "2049-2618",

publisher = "BioMed Central",

number = "1",

}

TY - JOUR

T1 - Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism

AU - Staley, Christopher

AU - Ferrieri, Abigail P.

AU - Tfaily, Malak M.

AU - Cui, Yaya

AU - Chu, Rosalie K.

AU - Wang, Ping

AU - Shaw, Jared B.

AU - Ansong, Charles K.

AU - Brewer, Heather

AU - Norbeck, Angela D.

AU - Markillie, Meng

AU - do Amaral, Fernanda

AU - Tuleski, Thalita

AU - Pellizzaro, Tomás

AU - Agtuca, Beverly

AU - Ferrieri, Richard

AU - Tringe, Susannah G.

AU - Paša-Tolić, Ljiljana

AU - Stacey, Gary

AU - Sadowsky, Michael J.

N1 - Funding Information: The work conducted by the DOE Joint Genome Institute and EMSL is supported by the Office of Science of the DOE under contract no. DE-AC02-05CH11231 (JGI) and DE-AC05-76RL01830 (EMSL). Work was also funded, in part, by a grant from the DOE Office of Science, Biological and Environmental Research (Grant No. DESC0013978 to GS). Funding Information: Special thanks to Dr. Rob McClung (Dartmouth Univ.) for providing seeds of the CCA1ox line. Sequence processing and analysis was performed, in part, using the resources of the Minnesota Supercomputing Institute. Mass spectrometry was performed using the Environmental and Molecular Sciences Laboratory (EMSL), a US Department of Energy (DOE) Office of Science User Facility sponsored by Biological and Environmental Research (BER) and located at Pacific Northwest National Laboratory (PNNL). PNNL is operated by Battelle for DOE.

PY - 2017/6/24

Y1 - 2017/6/24

N2 - BACKGROUND: 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.RESULTS: 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.CONCLUSIONS: 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.

AB - BACKGROUND: 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.RESULTS: 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.CONCLUSIONS: 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.

KW - Arabidopsis

KW - Bacterial community structure

KW - Diurnal rhythm

KW - Rhizosphere

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DO - 10.1186/s40168-017-0287-1

M3 - Article

C2 - 28646918

AN - SCOPUS:85040538905

SN - 2049-2618

VL - 5

SP - 65

JO - Microbiome

JF - Microbiome

IS - 1

ER -

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

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Keywords

ASJC Scopus subject areas

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