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Unexpected diversity during community succession in the apple flower microbiome.

Shade A, McManus PS, Handelsman J - MBio (2013)

Bottom Line: Yet fundamental knowledge of flower-associated microbiotas remains largely unknown.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut, USA.

ABSTRACT

Unlabelled: 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.

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Related in: MedlinePlus

Distribution and representation of apple flower microorganisms. The tree includes OTUs identified at least to the class level. The branch shading corresponds to the different phyla detected (phylum names indicated in boxes). The branch tip colors correspond to the successional groups of each taxon (OTUs with 97% tag sequence identity). The height and label of the colored bar indicate the relative abundance of each OTU in the data set, and unlabeled OTUs have relative abundances below 0.01. Note that Fig. 6 is a tool for visualizing the representation of OTUs among phyla and is not intended to depict evolutionary relationships.
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fig6: Distribution and representation of apple flower microorganisms. The tree includes OTUs identified at least to the class level. The branch shading corresponds to the different phyla detected (phylum names indicated in boxes). The branch tip colors correspond to the successional groups of each taxon (OTUs with 97% tag sequence identity). The height and label of the colored bar indicate the relative abundance of each OTU in the data set, and unlabeled OTUs have relative abundances below 0.01. Note that Fig. 6 is a tool for visualizing the representation of OTUs among phyla and is not intended to depict evolutionary relationships.

Mentions: OTUs of unidentified bacteria were prevalent in all groups, and TM7 and Deinococcus-Thermus OTUs were prevalent in five of the six groups (Table 1). We explored the phylogenetic distribution of successional group members and found that no one phylogenetic lineage was particularly abundant in any group (Fig. 6) except that some taxa affiliated with TM7 were more common in Early succession than at other stages.


Unexpected diversity during community succession in the apple flower microbiome.

Shade A, McManus PS, Handelsman J - MBio (2013)

Distribution and representation of apple flower microorganisms. The tree includes OTUs identified at least to the class level. The branch shading corresponds to the different phyla detected (phylum names indicated in boxes). The branch tip colors correspond to the successional groups of each taxon (OTUs with 97% tag sequence identity). The height and label of the colored bar indicate the relative abundance of each OTU in the data set, and unlabeled OTUs have relative abundances below 0.01. Note that Fig. 6 is a tool for visualizing the representation of OTUs among phyla and is not intended to depict evolutionary relationships.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3585449&req=5

fig6: Distribution and representation of apple flower microorganisms. The tree includes OTUs identified at least to the class level. The branch shading corresponds to the different phyla detected (phylum names indicated in boxes). The branch tip colors correspond to the successional groups of each taxon (OTUs with 97% tag sequence identity). The height and label of the colored bar indicate the relative abundance of each OTU in the data set, and unlabeled OTUs have relative abundances below 0.01. Note that Fig. 6 is a tool for visualizing the representation of OTUs among phyla and is not intended to depict evolutionary relationships.
Mentions: OTUs of unidentified bacteria were prevalent in all groups, and TM7 and Deinococcus-Thermus OTUs were prevalent in five of the six groups (Table 1). We explored the phylogenetic distribution of successional group members and found that no one phylogenetic lineage was particularly abundant in any group (Fig. 6) except that some taxa affiliated with TM7 were more common in Early succession than at other stages.

Bottom Line: Yet fundamental knowledge of flower-associated microbiotas remains largely unknown.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut, USA.

ABSTRACT

Unlabelled: 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.

Show MeSH
Related in: MedlinePlus