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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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Discovery, dynamics, and characteristics of apple flower successional groups. (a) Hierarchical clustering (complete linkage-based Bray-Curtis similarities among OTUs defined at 97% sequence identity) to determine OTUs having coherent dynamics. The analysis was conducted on 1,677 OTUs, each represented as a branch tip of the dendrogram. The y axis height represents within-cluster Bray-Curtis similarity. (b) Successional group dynamics indicating the mean relative abundance of members belonging to each group over the lifetime of apple flowers. Error bars indicate the standard deviation around the mean of 6 trees.
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fig4: Discovery, dynamics, and characteristics of apple flower successional groups. (a) Hierarchical clustering (complete linkage-based Bray-Curtis similarities among OTUs defined at 97% sequence identity) to determine OTUs having coherent dynamics. The analysis was conducted on 1,677 OTUs, each represented as a branch tip of the dendrogram. The y axis height represents within-cluster Bray-Curtis similarity. (b) Successional group dynamics indicating the mean relative abundance of members belonging to each group over the lifetime of apple flowers. Error bars indicate the standard deviation around the mean of 6 trees.

Mentions: Modest phylum-level changes in the community (see Fig. S1 in the supplemental material) suggested that the observed temporal patterns (Fig. 3) may be more apparent at the family, genus, or OTU level than at the phylum level. We hypothesized that there were groups of OTUs that had similar occurrence patterns, but we realized that these patterns may encompass a variety of distinct taxon dynamics (Fig. S2A posted at http://www.yale.edu/handelsmanlab/resources/index.html). To uncover possible trajectories, we performed a hierarchical cluster analysis to identify cooccurring taxa (supplemental methods in Text S1 and Fig. S3A posted at http://www.yale.edu/handelsmanlab/resources/index.html). We found that coherent occurrence patterns of OTUs on apple flowers were well described by the six most aggregated clusters (Fig. 4a). Furthermore, the peak abundances of the OTUs within these clusters occurred at different sampling times (Fig. 4b), and this temporal pattern was repeatable across trees, as indicated by the small error bars around the mean of six trees (Fig. 4b). We examined dynamics of each of the five most prevalent OTUs within each cluster and observed incremental increases and decreases of their abundances through time (Fig. 5). These patterns reflect the dynamics that define succession (Fig. S2A, panel f). Therefore, from these clusters we designated “successional groups” of OTUs that had coherent dynamics and distinct maxima at particular sampling times.


Unexpected diversity during community succession in the apple flower microbiome.

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

Discovery, dynamics, and characteristics of apple flower successional groups. (a) Hierarchical clustering (complete linkage-based Bray-Curtis similarities among OTUs defined at 97% sequence identity) to determine OTUs having coherent dynamics. The analysis was conducted on 1,677 OTUs, each represented as a branch tip of the dendrogram. The y axis height represents within-cluster Bray-Curtis similarity. (b) Successional group dynamics indicating the mean relative abundance of members belonging to each group over the lifetime of apple flowers. Error bars indicate the standard deviation around the mean of 6 trees.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig4: Discovery, dynamics, and characteristics of apple flower successional groups. (a) Hierarchical clustering (complete linkage-based Bray-Curtis similarities among OTUs defined at 97% sequence identity) to determine OTUs having coherent dynamics. The analysis was conducted on 1,677 OTUs, each represented as a branch tip of the dendrogram. The y axis height represents within-cluster Bray-Curtis similarity. (b) Successional group dynamics indicating the mean relative abundance of members belonging to each group over the lifetime of apple flowers. Error bars indicate the standard deviation around the mean of 6 trees.
Mentions: Modest phylum-level changes in the community (see Fig. S1 in the supplemental material) suggested that the observed temporal patterns (Fig. 3) may be more apparent at the family, genus, or OTU level than at the phylum level. We hypothesized that there were groups of OTUs that had similar occurrence patterns, but we realized that these patterns may encompass a variety of distinct taxon dynamics (Fig. S2A posted at http://www.yale.edu/handelsmanlab/resources/index.html). To uncover possible trajectories, we performed a hierarchical cluster analysis to identify cooccurring taxa (supplemental methods in Text S1 and Fig. S3A posted at http://www.yale.edu/handelsmanlab/resources/index.html). We found that coherent occurrence patterns of OTUs on apple flowers were well described by the six most aggregated clusters (Fig. 4a). Furthermore, the peak abundances of the OTUs within these clusters occurred at different sampling times (Fig. 4b), and this temporal pattern was repeatable across trees, as indicated by the small error bars around the mean of six trees (Fig. 4b). We examined dynamics of each of the five most prevalent OTUs within each cluster and observed incremental increases and decreases of their abundances through time (Fig. 5). These patterns reflect the dynamics that define succession (Fig. S2A, panel f). Therefore, from these clusters we designated “successional groups” of OTUs that had coherent dynamics and distinct maxima at particular sampling times.

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