The Leaf Microbiome of Arabidopsis Displays Reproducible Dynamics and Patterns throughout the Growing Season
ABSTRACT Leaves are primarily responsible for the plant’s photosynthetic activity. Thus, changes in the leaf microbiota, which includes deleterious and beneficial microbes, can have far-reaching effects on plant fitness and productivity. Identifying the processes and microorganisms that drive these...
Ausführliche Beschreibung
Autor*in: |
Juliana Almario [verfasserIn] Maryam Mahmoudi [verfasserIn] Samuel Kroll [verfasserIn] Mathew Agler [verfasserIn] Aleksandra Placzek [verfasserIn] Alfredo Mari [verfasserIn] Eric Kemen [verfasserIn] |
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E-Artikel |
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Sprache: |
Englisch |
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2022 |
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Übergeordnetes Werk: |
In: mBio - American Society for Microbiology, 2010, 13(2022), 3 |
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Übergeordnetes Werk: |
volume:13 ; year:2022 ; number:3 |
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DOI / URN: |
10.1128/mbio.02825-21 |
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Katalog-ID: |
DOAJ042405203 |
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10.1128/mbio.02825-21 doi (DE-627)DOAJ042405203 (DE-599)DOAJ93ceb88439c841e2a923dd85dfa121b0 DE-627 ger DE-627 rakwb eng QR1-502 Juliana Almario verfasserin aut The Leaf Microbiome of Arabidopsis Displays Reproducible Dynamics and Patterns throughout the Growing Season 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT Leaves are primarily responsible for the plant’s photosynthetic activity. Thus, changes in the leaf microbiota, which includes deleterious and beneficial microbes, can have far-reaching effects on plant fitness and productivity. Identifying the processes and microorganisms that drive these changes over a plant’s lifetime is, therefore, crucial. In this study, we analyzed the temporal dynamics in the leaf microbiome of Arabidopsis thaliana, integrating changes in both composition and microbe-microbe interactions via the study of microbial networks. Field-grown Arabidopsis were used to monitor leaf bacterial, fungal and oomycete communities throughout the plant’s natural growing season (extending from November to March) over three consecutive years. Our results revealed the existence of conserved temporal patterns, with microbial communities and networks going through a stabilization phase of decreased diversity and variability at the beginning of the plant’s growing season. Despite a high turnover in these communities, we identified 19 “core” taxa persisting on Arabidopsis leaves across time and plant generations. With the hypothesis these microbes could be playing key roles in the structuring of leaf microbial communities, we conducted a time-informed microbial network analysis which showed core taxa are not necessarily highly connected network “hubs,” and “hubs” alternate with time. Our study shows that leaf microbial communities exhibit reproducible dynamics and patterns, suggesting the potential of using our understanding of temporal trajectories in microbial community composition to design experiments aimed at driving these communities toward desired states. IMPORTANCE Utilizing plant microbiota to promote plant growth and plant health is key to more environmentally friendly agriculture. A major bottleneck in the engineering of plant-beneficial microbial communities is the low persistence of applied microbes under filed conditions, especially considering plant leaves. Indeed, although many leaf-associated microorganisms have the potential to promote plant growth and protect plants from pathogens, few of them are able to survive and thrive over time. In our study, we could show that leaf microbial communities are very variable at the beginning of the plant growing season but become more and more similar and less variable as the season progresses. We further identify a cohort of 19 “core” microbes, systematically present on plant leaves that would make these microbes exceptional candidates for future agricultural applications. leaf microbiome time dynamics microbial networks microbial hubs community dynamics core microbial community Microbiology Maryam Mahmoudi verfasserin aut Samuel Kroll verfasserin aut Mathew Agler verfasserin aut Aleksandra Placzek verfasserin aut Alfredo Mari verfasserin aut Eric Kemen verfasserin aut In mBio American Society for Microbiology, 2010 13(2022), 3 (DE-627)627613543 (DE-600)2557172-2 21507511 nnns volume:13 year:2022 number:3 https://doi.org/10.1128/mbio.02825-21 kostenfrei https://doaj.org/article/93ceb88439c841e2a923dd85dfa121b0 kostenfrei https://journals.asm.org/doi/10.1128/mbio.02825-21 kostenfrei https://doaj.org/toc/2150-7511 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 13 2022 3 |
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10.1128/mbio.02825-21 doi (DE-627)DOAJ042405203 (DE-599)DOAJ93ceb88439c841e2a923dd85dfa121b0 DE-627 ger DE-627 rakwb eng QR1-502 Juliana Almario verfasserin aut The Leaf Microbiome of Arabidopsis Displays Reproducible Dynamics and Patterns throughout the Growing Season 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT Leaves are primarily responsible for the plant’s photosynthetic activity. Thus, changes in the leaf microbiota, which includes deleterious and beneficial microbes, can have far-reaching effects on plant fitness and productivity. Identifying the processes and microorganisms that drive these changes over a plant’s lifetime is, therefore, crucial. In this study, we analyzed the temporal dynamics in the leaf microbiome of Arabidopsis thaliana, integrating changes in both composition and microbe-microbe interactions via the study of microbial networks. Field-grown Arabidopsis were used to monitor leaf bacterial, fungal and oomycete communities throughout the plant’s natural growing season (extending from November to March) over three consecutive years. Our results revealed the existence of conserved temporal patterns, with microbial communities and networks going through a stabilization phase of decreased diversity and variability at the beginning of the plant’s growing season. Despite a high turnover in these communities, we identified 19 “core” taxa persisting on Arabidopsis leaves across time and plant generations. With the hypothesis these microbes could be playing key roles in the structuring of leaf microbial communities, we conducted a time-informed microbial network analysis which showed core taxa are not necessarily highly connected network “hubs,” and “hubs” alternate with time. Our study shows that leaf microbial communities exhibit reproducible dynamics and patterns, suggesting the potential of using our understanding of temporal trajectories in microbial community composition to design experiments aimed at driving these communities toward desired states. IMPORTANCE Utilizing plant microbiota to promote plant growth and plant health is key to more environmentally friendly agriculture. A major bottleneck in the engineering of plant-beneficial microbial communities is the low persistence of applied microbes under filed conditions, especially considering plant leaves. Indeed, although many leaf-associated microorganisms have the potential to promote plant growth and protect plants from pathogens, few of them are able to survive and thrive over time. In our study, we could show that leaf microbial communities are very variable at the beginning of the plant growing season but become more and more similar and less variable as the season progresses. We further identify a cohort of 19 “core” microbes, systematically present on plant leaves that would make these microbes exceptional candidates for future agricultural applications. leaf microbiome time dynamics microbial networks microbial hubs community dynamics core microbial community Microbiology Maryam Mahmoudi verfasserin aut Samuel Kroll verfasserin aut Mathew Agler verfasserin aut Aleksandra Placzek verfasserin aut Alfredo Mari verfasserin aut Eric Kemen verfasserin aut In mBio American Society for Microbiology, 2010 13(2022), 3 (DE-627)627613543 (DE-600)2557172-2 21507511 nnns volume:13 year:2022 number:3 https://doi.org/10.1128/mbio.02825-21 kostenfrei https://doaj.org/article/93ceb88439c841e2a923dd85dfa121b0 kostenfrei https://journals.asm.org/doi/10.1128/mbio.02825-21 kostenfrei https://doaj.org/toc/2150-7511 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 13 2022 3 |
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10.1128/mbio.02825-21 doi (DE-627)DOAJ042405203 (DE-599)DOAJ93ceb88439c841e2a923dd85dfa121b0 DE-627 ger DE-627 rakwb eng QR1-502 Juliana Almario verfasserin aut The Leaf Microbiome of Arabidopsis Displays Reproducible Dynamics and Patterns throughout the Growing Season 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT Leaves are primarily responsible for the plant’s photosynthetic activity. Thus, changes in the leaf microbiota, which includes deleterious and beneficial microbes, can have far-reaching effects on plant fitness and productivity. Identifying the processes and microorganisms that drive these changes over a plant’s lifetime is, therefore, crucial. In this study, we analyzed the temporal dynamics in the leaf microbiome of Arabidopsis thaliana, integrating changes in both composition and microbe-microbe interactions via the study of microbial networks. Field-grown Arabidopsis were used to monitor leaf bacterial, fungal and oomycete communities throughout the plant’s natural growing season (extending from November to March) over three consecutive years. Our results revealed the existence of conserved temporal patterns, with microbial communities and networks going through a stabilization phase of decreased diversity and variability at the beginning of the plant’s growing season. Despite a high turnover in these communities, we identified 19 “core” taxa persisting on Arabidopsis leaves across time and plant generations. With the hypothesis these microbes could be playing key roles in the structuring of leaf microbial communities, we conducted a time-informed microbial network analysis which showed core taxa are not necessarily highly connected network “hubs,” and “hubs” alternate with time. Our study shows that leaf microbial communities exhibit reproducible dynamics and patterns, suggesting the potential of using our understanding of temporal trajectories in microbial community composition to design experiments aimed at driving these communities toward desired states. IMPORTANCE Utilizing plant microbiota to promote plant growth and plant health is key to more environmentally friendly agriculture. A major bottleneck in the engineering of plant-beneficial microbial communities is the low persistence of applied microbes under filed conditions, especially considering plant leaves. Indeed, although many leaf-associated microorganisms have the potential to promote plant growth and protect plants from pathogens, few of them are able to survive and thrive over time. In our study, we could show that leaf microbial communities are very variable at the beginning of the plant growing season but become more and more similar and less variable as the season progresses. We further identify a cohort of 19 “core” microbes, systematically present on plant leaves that would make these microbes exceptional candidates for future agricultural applications. leaf microbiome time dynamics microbial networks microbial hubs community dynamics core microbial community Microbiology Maryam Mahmoudi verfasserin aut Samuel Kroll verfasserin aut Mathew Agler verfasserin aut Aleksandra Placzek verfasserin aut Alfredo Mari verfasserin aut Eric Kemen verfasserin aut In mBio American Society for Microbiology, 2010 13(2022), 3 (DE-627)627613543 (DE-600)2557172-2 21507511 nnns volume:13 year:2022 number:3 https://doi.org/10.1128/mbio.02825-21 kostenfrei https://doaj.org/article/93ceb88439c841e2a923dd85dfa121b0 kostenfrei https://journals.asm.org/doi/10.1128/mbio.02825-21 kostenfrei https://doaj.org/toc/2150-7511 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 13 2022 3 |
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10.1128/mbio.02825-21 doi (DE-627)DOAJ042405203 (DE-599)DOAJ93ceb88439c841e2a923dd85dfa121b0 DE-627 ger DE-627 rakwb eng QR1-502 Juliana Almario verfasserin aut The Leaf Microbiome of Arabidopsis Displays Reproducible Dynamics and Patterns throughout the Growing Season 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT Leaves are primarily responsible for the plant’s photosynthetic activity. Thus, changes in the leaf microbiota, which includes deleterious and beneficial microbes, can have far-reaching effects on plant fitness and productivity. Identifying the processes and microorganisms that drive these changes over a plant’s lifetime is, therefore, crucial. In this study, we analyzed the temporal dynamics in the leaf microbiome of Arabidopsis thaliana, integrating changes in both composition and microbe-microbe interactions via the study of microbial networks. Field-grown Arabidopsis were used to monitor leaf bacterial, fungal and oomycete communities throughout the plant’s natural growing season (extending from November to March) over three consecutive years. Our results revealed the existence of conserved temporal patterns, with microbial communities and networks going through a stabilization phase of decreased diversity and variability at the beginning of the plant’s growing season. Despite a high turnover in these communities, we identified 19 “core” taxa persisting on Arabidopsis leaves across time and plant generations. With the hypothesis these microbes could be playing key roles in the structuring of leaf microbial communities, we conducted a time-informed microbial network analysis which showed core taxa are not necessarily highly connected network “hubs,” and “hubs” alternate with time. Our study shows that leaf microbial communities exhibit reproducible dynamics and patterns, suggesting the potential of using our understanding of temporal trajectories in microbial community composition to design experiments aimed at driving these communities toward desired states. IMPORTANCE Utilizing plant microbiota to promote plant growth and plant health is key to more environmentally friendly agriculture. A major bottleneck in the engineering of plant-beneficial microbial communities is the low persistence of applied microbes under filed conditions, especially considering plant leaves. Indeed, although many leaf-associated microorganisms have the potential to promote plant growth and protect plants from pathogens, few of them are able to survive and thrive over time. In our study, we could show that leaf microbial communities are very variable at the beginning of the plant growing season but become more and more similar and less variable as the season progresses. We further identify a cohort of 19 “core” microbes, systematically present on plant leaves that would make these microbes exceptional candidates for future agricultural applications. leaf microbiome time dynamics microbial networks microbial hubs community dynamics core microbial community Microbiology Maryam Mahmoudi verfasserin aut Samuel Kroll verfasserin aut Mathew Agler verfasserin aut Aleksandra Placzek verfasserin aut Alfredo Mari verfasserin aut Eric Kemen verfasserin aut In mBio American Society for Microbiology, 2010 13(2022), 3 (DE-627)627613543 (DE-600)2557172-2 21507511 nnns volume:13 year:2022 number:3 https://doi.org/10.1128/mbio.02825-21 kostenfrei https://doaj.org/article/93ceb88439c841e2a923dd85dfa121b0 kostenfrei https://journals.asm.org/doi/10.1128/mbio.02825-21 kostenfrei https://doaj.org/toc/2150-7511 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 13 2022 3 |
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10.1128/mbio.02825-21 doi (DE-627)DOAJ042405203 (DE-599)DOAJ93ceb88439c841e2a923dd85dfa121b0 DE-627 ger DE-627 rakwb eng QR1-502 Juliana Almario verfasserin aut The Leaf Microbiome of Arabidopsis Displays Reproducible Dynamics and Patterns throughout the Growing Season 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT Leaves are primarily responsible for the plant’s photosynthetic activity. Thus, changes in the leaf microbiota, which includes deleterious and beneficial microbes, can have far-reaching effects on plant fitness and productivity. Identifying the processes and microorganisms that drive these changes over a plant’s lifetime is, therefore, crucial. In this study, we analyzed the temporal dynamics in the leaf microbiome of Arabidopsis thaliana, integrating changes in both composition and microbe-microbe interactions via the study of microbial networks. Field-grown Arabidopsis were used to monitor leaf bacterial, fungal and oomycete communities throughout the plant’s natural growing season (extending from November to March) over three consecutive years. Our results revealed the existence of conserved temporal patterns, with microbial communities and networks going through a stabilization phase of decreased diversity and variability at the beginning of the plant’s growing season. Despite a high turnover in these communities, we identified 19 “core” taxa persisting on Arabidopsis leaves across time and plant generations. With the hypothesis these microbes could be playing key roles in the structuring of leaf microbial communities, we conducted a time-informed microbial network analysis which showed core taxa are not necessarily highly connected network “hubs,” and “hubs” alternate with time. Our study shows that leaf microbial communities exhibit reproducible dynamics and patterns, suggesting the potential of using our understanding of temporal trajectories in microbial community composition to design experiments aimed at driving these communities toward desired states. IMPORTANCE Utilizing plant microbiota to promote plant growth and plant health is key to more environmentally friendly agriculture. A major bottleneck in the engineering of plant-beneficial microbial communities is the low persistence of applied microbes under filed conditions, especially considering plant leaves. Indeed, although many leaf-associated microorganisms have the potential to promote plant growth and protect plants from pathogens, few of them are able to survive and thrive over time. In our study, we could show that leaf microbial communities are very variable at the beginning of the plant growing season but become more and more similar and less variable as the season progresses. We further identify a cohort of 19 “core” microbes, systematically present on plant leaves that would make these microbes exceptional candidates for future agricultural applications. leaf microbiome time dynamics microbial networks microbial hubs community dynamics core microbial community Microbiology Maryam Mahmoudi verfasserin aut Samuel Kroll verfasserin aut Mathew Agler verfasserin aut Aleksandra Placzek verfasserin aut Alfredo Mari verfasserin aut Eric Kemen verfasserin aut In mBio American Society for Microbiology, 2010 13(2022), 3 (DE-627)627613543 (DE-600)2557172-2 21507511 nnns volume:13 year:2022 number:3 https://doi.org/10.1128/mbio.02825-21 kostenfrei https://doaj.org/article/93ceb88439c841e2a923dd85dfa121b0 kostenfrei https://journals.asm.org/doi/10.1128/mbio.02825-21 kostenfrei https://doaj.org/toc/2150-7511 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 13 2022 3 |
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The Leaf Microbiome of Arabidopsis Displays Reproducible Dynamics and Patterns throughout the Growing Season |
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ABSTRACT Leaves are primarily responsible for the plant’s photosynthetic activity. Thus, changes in the leaf microbiota, which includes deleterious and beneficial microbes, can have far-reaching effects on plant fitness and productivity. Identifying the processes and microorganisms that drive these changes over a plant’s lifetime is, therefore, crucial. In this study, we analyzed the temporal dynamics in the leaf microbiome of Arabidopsis thaliana, integrating changes in both composition and microbe-microbe interactions via the study of microbial networks. Field-grown Arabidopsis were used to monitor leaf bacterial, fungal and oomycete communities throughout the plant’s natural growing season (extending from November to March) over three consecutive years. Our results revealed the existence of conserved temporal patterns, with microbial communities and networks going through a stabilization phase of decreased diversity and variability at the beginning of the plant’s growing season. Despite a high turnover in these communities, we identified 19 “core” taxa persisting on Arabidopsis leaves across time and plant generations. With the hypothesis these microbes could be playing key roles in the structuring of leaf microbial communities, we conducted a time-informed microbial network analysis which showed core taxa are not necessarily highly connected network “hubs,” and “hubs” alternate with time. Our study shows that leaf microbial communities exhibit reproducible dynamics and patterns, suggesting the potential of using our understanding of temporal trajectories in microbial community composition to design experiments aimed at driving these communities toward desired states. IMPORTANCE Utilizing plant microbiota to promote plant growth and plant health is key to more environmentally friendly agriculture. A major bottleneck in the engineering of plant-beneficial microbial communities is the low persistence of applied microbes under filed conditions, especially considering plant leaves. Indeed, although many leaf-associated microorganisms have the potential to promote plant growth and protect plants from pathogens, few of them are able to survive and thrive over time. In our study, we could show that leaf microbial communities are very variable at the beginning of the plant growing season but become more and more similar and less variable as the season progresses. We further identify a cohort of 19 “core” microbes, systematically present on plant leaves that would make these microbes exceptional candidates for future agricultural applications. |
abstractGer |
ABSTRACT Leaves are primarily responsible for the plant’s photosynthetic activity. Thus, changes in the leaf microbiota, which includes deleterious and beneficial microbes, can have far-reaching effects on plant fitness and productivity. Identifying the processes and microorganisms that drive these changes over a plant’s lifetime is, therefore, crucial. In this study, we analyzed the temporal dynamics in the leaf microbiome of Arabidopsis thaliana, integrating changes in both composition and microbe-microbe interactions via the study of microbial networks. Field-grown Arabidopsis were used to monitor leaf bacterial, fungal and oomycete communities throughout the plant’s natural growing season (extending from November to March) over three consecutive years. Our results revealed the existence of conserved temporal patterns, with microbial communities and networks going through a stabilization phase of decreased diversity and variability at the beginning of the plant’s growing season. Despite a high turnover in these communities, we identified 19 “core” taxa persisting on Arabidopsis leaves across time and plant generations. With the hypothesis these microbes could be playing key roles in the structuring of leaf microbial communities, we conducted a time-informed microbial network analysis which showed core taxa are not necessarily highly connected network “hubs,” and “hubs” alternate with time. Our study shows that leaf microbial communities exhibit reproducible dynamics and patterns, suggesting the potential of using our understanding of temporal trajectories in microbial community composition to design experiments aimed at driving these communities toward desired states. IMPORTANCE Utilizing plant microbiota to promote plant growth and plant health is key to more environmentally friendly agriculture. A major bottleneck in the engineering of plant-beneficial microbial communities is the low persistence of applied microbes under filed conditions, especially considering plant leaves. Indeed, although many leaf-associated microorganisms have the potential to promote plant growth and protect plants from pathogens, few of them are able to survive and thrive over time. In our study, we could show that leaf microbial communities are very variable at the beginning of the plant growing season but become more and more similar and less variable as the season progresses. We further identify a cohort of 19 “core” microbes, systematically present on plant leaves that would make these microbes exceptional candidates for future agricultural applications. |
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ABSTRACT Leaves are primarily responsible for the plant’s photosynthetic activity. Thus, changes in the leaf microbiota, which includes deleterious and beneficial microbes, can have far-reaching effects on plant fitness and productivity. Identifying the processes and microorganisms that drive these changes over a plant’s lifetime is, therefore, crucial. In this study, we analyzed the temporal dynamics in the leaf microbiome of Arabidopsis thaliana, integrating changes in both composition and microbe-microbe interactions via the study of microbial networks. Field-grown Arabidopsis were used to monitor leaf bacterial, fungal and oomycete communities throughout the plant’s natural growing season (extending from November to March) over three consecutive years. Our results revealed the existence of conserved temporal patterns, with microbial communities and networks going through a stabilization phase of decreased diversity and variability at the beginning of the plant’s growing season. Despite a high turnover in these communities, we identified 19 “core” taxa persisting on Arabidopsis leaves across time and plant generations. With the hypothesis these microbes could be playing key roles in the structuring of leaf microbial communities, we conducted a time-informed microbial network analysis which showed core taxa are not necessarily highly connected network “hubs,” and “hubs” alternate with time. Our study shows that leaf microbial communities exhibit reproducible dynamics and patterns, suggesting the potential of using our understanding of temporal trajectories in microbial community composition to design experiments aimed at driving these communities toward desired states. IMPORTANCE Utilizing plant microbiota to promote plant growth and plant health is key to more environmentally friendly agriculture. A major bottleneck in the engineering of plant-beneficial microbial communities is the low persistence of applied microbes under filed conditions, especially considering plant leaves. Indeed, although many leaf-associated microorganisms have the potential to promote plant growth and protect plants from pathogens, few of them are able to survive and thrive over time. In our study, we could show that leaf microbial communities are very variable at the beginning of the plant growing season but become more and more similar and less variable as the season progresses. We further identify a cohort of 19 “core” microbes, systematically present on plant leaves that would make these microbes exceptional candidates for future agricultural applications. |
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<?xml version="1.0" encoding="UTF-8"?><collection xmlns="http://www.loc.gov/MARC21/slim"><record><leader>01000caa a22002652 4500</leader><controlfield tag="001">DOAJ042405203</controlfield><controlfield tag="003">DE-627</controlfield><controlfield tag="005">20230308061140.0</controlfield><controlfield tag="007">cr uuu---uuuuu</controlfield><controlfield tag="008">230227s2022 xx |||||o 00| ||eng c</controlfield><datafield tag="024" ind1="7" ind2=" "><subfield code="a">10.1128/mbio.02825-21</subfield><subfield code="2">doi</subfield></datafield><datafield tag="035" ind1=" " ind2=" "><subfield code="a">(DE-627)DOAJ042405203</subfield></datafield><datafield tag="035" ind1=" " ind2=" "><subfield code="a">(DE-599)DOAJ93ceb88439c841e2a923dd85dfa121b0</subfield></datafield><datafield tag="040" ind1=" " ind2=" "><subfield code="a">DE-627</subfield><subfield code="b">ger</subfield><subfield code="c">DE-627</subfield><subfield code="e">rakwb</subfield></datafield><datafield tag="041" ind1=" " ind2=" "><subfield code="a">eng</subfield></datafield><datafield tag="050" ind1=" " ind2="0"><subfield code="a">QR1-502</subfield></datafield><datafield tag="100" ind1="0" ind2=" "><subfield code="a">Juliana Almario</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="245" ind1="1" ind2="4"><subfield code="a">The Leaf Microbiome of Arabidopsis Displays Reproducible Dynamics and Patterns throughout the Growing Season</subfield></datafield><datafield tag="264" ind1=" " ind2="1"><subfield code="c">2022</subfield></datafield><datafield tag="336" ind1=" " ind2=" "><subfield code="a">Text</subfield><subfield code="b">txt</subfield><subfield code="2">rdacontent</subfield></datafield><datafield tag="337" ind1=" " ind2=" "><subfield code="a">Computermedien</subfield><subfield code="b">c</subfield><subfield code="2">rdamedia</subfield></datafield><datafield tag="338" ind1=" " ind2=" "><subfield code="a">Online-Ressource</subfield><subfield code="b">cr</subfield><subfield code="2">rdacarrier</subfield></datafield><datafield tag="520" ind1=" " ind2=" "><subfield code="a">ABSTRACT Leaves are primarily responsible for the plant’s photosynthetic activity. Thus, changes in the leaf microbiota, which includes deleterious and beneficial microbes, can have far-reaching effects on plant fitness and productivity. Identifying the processes and microorganisms that drive these changes over a plant’s lifetime is, therefore, crucial. In this study, we analyzed the temporal dynamics in the leaf microbiome of Arabidopsis thaliana, integrating changes in both composition and microbe-microbe interactions via the study of microbial networks. Field-grown Arabidopsis were used to monitor leaf bacterial, fungal and oomycete communities throughout the plant’s natural growing season (extending from November to March) over three consecutive years. Our results revealed the existence of conserved temporal patterns, with microbial communities and networks going through a stabilization phase of decreased diversity and variability at the beginning of the plant’s growing season. Despite a high turnover in these communities, we identified 19 “core” taxa persisting on Arabidopsis leaves across time and plant generations. With the hypothesis these microbes could be playing key roles in the structuring of leaf microbial communities, we conducted a time-informed microbial network analysis which showed core taxa are not necessarily highly connected network “hubs,” and “hubs” alternate with time. Our study shows that leaf microbial communities exhibit reproducible dynamics and patterns, suggesting the potential of using our understanding of temporal trajectories in microbial community composition to design experiments aimed at driving these communities toward desired states. IMPORTANCE Utilizing plant microbiota to promote plant growth and plant health is key to more environmentally friendly agriculture. A major bottleneck in the engineering of plant-beneficial microbial communities is the low persistence of applied microbes under filed conditions, especially considering plant leaves. Indeed, although many leaf-associated microorganisms have the potential to promote plant growth and protect plants from pathogens, few of them are able to survive and thrive over time. In our study, we could show that leaf microbial communities are very variable at the beginning of the plant growing season but become more and more similar and less variable as the season progresses. We further identify a cohort of 19 “core” microbes, systematically present on plant leaves that would make these microbes exceptional candidates for future agricultural applications.</subfield></datafield><datafield tag="650" ind1=" " ind2="4"><subfield code="a">leaf microbiome</subfield></datafield><datafield tag="650" ind1=" " ind2="4"><subfield code="a">time dynamics</subfield></datafield><datafield tag="650" ind1=" " ind2="4"><subfield code="a">microbial networks</subfield></datafield><datafield tag="650" ind1=" " ind2="4"><subfield code="a">microbial hubs</subfield></datafield><datafield tag="650" ind1=" " ind2="4"><subfield code="a">community dynamics</subfield></datafield><datafield tag="650" ind1=" " ind2="4"><subfield code="a">core microbial community</subfield></datafield><datafield tag="653" ind1=" " ind2="0"><subfield code="a">Microbiology</subfield></datafield><datafield tag="700" ind1="0" ind2=" "><subfield code="a">Maryam Mahmoudi</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="0" ind2=" "><subfield code="a">Samuel Kroll</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="0" ind2=" "><subfield code="a">Mathew Agler</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="0" ind2=" "><subfield code="a">Aleksandra Placzek</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="0" ind2=" "><subfield code="a">Alfredo Mari</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="0" ind2=" "><subfield code="a">Eric Kemen</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="773" ind1="0" ind2="8"><subfield code="i">In</subfield><subfield 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