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 s...
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| Format: | Article |
| Language: | English |
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BMC
2017-06-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s40168-017-0287-1 |
| _version_ | 1819211410539806720 |
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| author | 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 |
| author_facet | 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 |
| author_sort | Christopher Staley |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-23T06:26:38Z |
| format | Article |
| id | doaj.art-4731b83b0f9a459195c19745a09b71e8 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-12-23T06:26:38Z |
| publishDate | 2017-06-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-4731b83b0f9a459195c19745a09b71e82022-12-21T17:57:03ZengBMCMicrobiome2049-26182017-06-015111310.1186/s40168-017-0287-1Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolismChristopher Staley0Abigail P. Ferrieri1Malak M. Tfaily2Yaya Cui3Rosalie K. Chu4Ping Wang5Jared B. Shaw6Charles K. Ansong7Heather Brewer8Angela D. Norbeck9Meng Markillie10Fernanda do Amaral11Thalita Tuleski12Tomás Pellizzaro13Beverly Agtuca14Richard Ferrieri15Susannah G. Tringe16Ljiljana Paša-Tolić17Gary Stacey18Michael J. Sadowsky19BioTechnology Institute, University of MinnesotaEnvironmental Molecular Sciences Laboratory, Pacific Northwest National LaboratoryEnvironmental Molecular Sciences Laboratory, Pacific Northwest National LaboratoryDivision of Plant Science and Biochemistry, C.S. Bond Life Science Center, University of MissouriEnvironmental Molecular Sciences Laboratory, Pacific Northwest National LaboratoryBioTechnology Institute, University of MinnesotaEnvironmental Molecular Sciences Laboratory, Pacific Northwest National LaboratoryBiological Sciences Division, Pacific Northwest National LaboratoryEnvironmental Molecular Sciences Laboratory, Pacific Northwest National LaboratoryEnvironmental Molecular Sciences Laboratory, Pacific Northwest National LaboratoryEnvironmental Molecular Sciences Laboratory, Pacific Northwest National LaboratoryDivision of Plant Science and Biochemistry, C.S. Bond Life Science Center, University of MissouriDivision of Plant Science and Biochemistry, C.S. Bond Life Science Center, University of MissouriDivision of Plant Science and Biochemistry, C.S. Bond Life Science Center, University of MissouriDivision of Plant Science and Biochemistry, C.S. Bond Life Science Center, University of MissouriDepartment of Chemistry, University of Missouri Research ReactorMicrobial Systems Group, Metagenome Program, DOE Joint Genome InstituteEnvironmental Molecular Sciences Laboratory, Pacific Northwest National LaboratoryDivision of Plant Science and Biochemistry, C.S. Bond Life Science Center, University of MissouriBioTechnology Institute, University of MinnesotaAbstract 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.http://link.springer.com/article/10.1186/s40168-017-0287-1Bacterial community structureDiurnal rhythmRhizosphereArabidopsis |
| spellingShingle | 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 Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism Microbiome Bacterial community structure Diurnal rhythm Rhizosphere Arabidopsis |
| title | Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism |
| title_full | Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism |
| title_fullStr | Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism |
| title_full_unstemmed | Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism |
| title_short | Diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism |
| title_sort | diurnal cycling of rhizosphere bacterial communities is associated with shifts in carbon metabolism |
| topic | Bacterial community structure Diurnal rhythm Rhizosphere Arabidopsis |
| url | http://link.springer.com/article/10.1186/s40168-017-0287-1 |
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