Unexpected Diversity during Community Succession in the Apple Flower Microbiome

ABSTRACT Despite its importance to the host, the flower microbiome is poorly understood. We report a culture-independent, community-level assessment of apple flower microbial diversity and dynamics. We collected flowers from six apple trees at five time points, starting before flowers opened and end...

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Autores principales: Ashley Shade, Patricia S. McManus, Jo Handelsman
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Publicado: American Society for Microbiology 2013
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spelling oai:doaj.org-article:6c965aefa678466092820617ce1f49e12021-11-15T15:40:28ZUnexpected Diversity during Community Succession in the Apple Flower Microbiome10.1128/mBio.00602-122150-7511https://doaj.org/article/6c965aefa678466092820617ce1f49e12013-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00602-12https://doaj.org/toc/2150-7511ABSTRACT Despite its importance to the host, the flower microbiome is poorly understood. We report a culture-independent, community-level assessment of apple flower microbial diversity and dynamics. We collected flowers from six apple trees at five time points, starting before flowers opened and ending at petal fall. We applied streptomycin to half of the trees when flowers opened. Assessment of microbial diversity using tag pyrosequencing of 16S rRNA genes revealed that the apple flower communities were rich and diverse and dominated by members of TM7 and Deinococcus-Thermus, phyla about which relatively little is known. From thousands of taxa, we identified six successional groups with coherent dynamics whose abundances peaked at different times before and after bud opening. We designated the groups Pioneer, Early, Mid, Late, Climax, and Generalist communities. The successional pattern was attributed to a set of prevalent taxa that were persistent and gradually changing in abundance. These taxa had significant associations with other community members, as demonstrated with a cooccurrence network based on local similarity analysis. We also detected a set of less-abundant, transient taxa that contributed to general tree-to-tree variability but not to the successional pattern. Communities on trees sprayed with streptomycin had slightly lower phylogenetic diversity than those on unsprayed trees but did not differ in structure or succession. Our results suggest that changes in apple flower microbial community structure are predictable over the life of the flower, providing a basis for ecological understanding and disease management. IMPORTANCE Flowering plants (angiosperms) represent a diverse group of an estimated 400,000 species, and their successful cultivation is essential to agriculture. Yet fundamental knowledge of flower-associated microbiotas remains largely unknown. Even less well understood are the changes that flower microbial communities experience through time. Flowers are particularly conducive to comprehensive temporal studies because they are, by nature, ephemeral organs. Here, we present the first culture-independent time series of bacterial and archaeal communities associated with the flowers of apple, an economically important crop. We found unexpected diversity on apple flowers, including a preponderance of taxa affiliated with Deinococcus-Thermus and TM7, phyla that are understudied but thought to be tolerant to an array of environmental stresses. Our results also suggest that changes in microbial community structure on the apple flower may be predictable over the life of the flower, providing the basis for ecological understanding and disease management.Ashley ShadePatricia S. McManusJo HandelsmanAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 2 (2013)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Ashley Shade
Patricia S. McManus
Jo Handelsman
Unexpected Diversity during Community Succession in the Apple Flower Microbiome
description ABSTRACT Despite its importance to the host, the flower microbiome is poorly understood. We report a culture-independent, community-level assessment of apple flower microbial diversity and dynamics. We collected flowers from six apple trees at five time points, starting before flowers opened and ending at petal fall. We applied streptomycin to half of the trees when flowers opened. Assessment of microbial diversity using tag pyrosequencing of 16S rRNA genes revealed that the apple flower communities were rich and diverse and dominated by members of TM7 and Deinococcus-Thermus, phyla about which relatively little is known. From thousands of taxa, we identified six successional groups with coherent dynamics whose abundances peaked at different times before and after bud opening. We designated the groups Pioneer, Early, Mid, Late, Climax, and Generalist communities. The successional pattern was attributed to a set of prevalent taxa that were persistent and gradually changing in abundance. These taxa had significant associations with other community members, as demonstrated with a cooccurrence network based on local similarity analysis. We also detected a set of less-abundant, transient taxa that contributed to general tree-to-tree variability but not to the successional pattern. Communities on trees sprayed with streptomycin had slightly lower phylogenetic diversity than those on unsprayed trees but did not differ in structure or succession. Our results suggest that changes in apple flower microbial community structure are predictable over the life of the flower, providing a basis for ecological understanding and disease management. IMPORTANCE Flowering plants (angiosperms) represent a diverse group of an estimated 400,000 species, and their successful cultivation is essential to agriculture. Yet fundamental knowledge of flower-associated microbiotas remains largely unknown. Even less well understood are the changes that flower microbial communities experience through time. Flowers are particularly conducive to comprehensive temporal studies because they are, by nature, ephemeral organs. Here, we present the first culture-independent time series of bacterial and archaeal communities associated with the flowers of apple, an economically important crop. We found unexpected diversity on apple flowers, including a preponderance of taxa affiliated with Deinococcus-Thermus and TM7, phyla that are understudied but thought to be tolerant to an array of environmental stresses. Our results also suggest that changes in microbial community structure on the apple flower may be predictable over the life of the flower, providing the basis for ecological understanding and disease management.
format article
author Ashley Shade
Patricia S. McManus
Jo Handelsman
author_facet Ashley Shade
Patricia S. McManus
Jo Handelsman
author_sort Ashley Shade
title Unexpected Diversity during Community Succession in the Apple Flower Microbiome
title_short Unexpected Diversity during Community Succession in the Apple Flower Microbiome
title_full Unexpected Diversity during Community Succession in the Apple Flower Microbiome
title_fullStr Unexpected Diversity during Community Succession in the Apple Flower Microbiome
title_full_unstemmed Unexpected Diversity during Community Succession in the Apple Flower Microbiome
title_sort unexpected diversity during community succession in the apple flower microbiome
publisher American Society for Microbiology
publishDate 2013
url https://doaj.org/article/6c965aefa678466092820617ce1f49e1
work_keys_str_mv AT ashleyshade unexpecteddiversityduringcommunitysuccessionintheappleflowermicrobiome
AT patriciasmcmanus unexpecteddiversityduringcommunitysuccessionintheappleflowermicrobiome
AT johandelsman unexpecteddiversityduringcommunitysuccessionintheappleflowermicrobiome
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