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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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Temporal trends in the apple flower microbiome. For each time point, n = 6 (1 sample of DNA extracted in bulk from 15 flowers from each of six trees). The inner-quartile ranges are shown by the box boundaries, nonoutlier extremes are shown by the whiskers, the median is shown by the thick middle line, and outliers are shown by the outliers’ black points. Statistics were summarized across each of six trees sampled at each time point, and the communities were analyzed at the 97% OTU level. Trees 4, 5, and 6 were sprayed with streptomycin on 29 and 30 April 2010. (a) Rarefied Faith’s phylogenetic diversity of microorganisms. There were 10 resamples at a depth of 1,531 sequences for each tree at each time point. Letters indicate significant differences in phylogenetic diversity across days, assessed by analysis of variance (F = 101.56, 4 degrees of freedom [df], P < 0.001) and post hoc testing with Tukey’s HSD test (P < 0.05). (b) Variability in community structure (assessed by analysis of beta dispersion, a metric of variability). Though modest differences were detected (multivariate homogeneity of group dispersions; F = 2.34, 4 df, P = 0.08), a post hoc test revealed that only 27 and 29 April were different (Tukey’s HSD test; P = 0.09).
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fig3: Temporal trends in the apple flower microbiome. For each time point, n = 6 (1 sample of DNA extracted in bulk from 15 flowers from each of six trees). The inner-quartile ranges are shown by the box boundaries, nonoutlier extremes are shown by the whiskers, the median is shown by the thick middle line, and outliers are shown by the outliers’ black points. Statistics were summarized across each of six trees sampled at each time point, and the communities were analyzed at the 97% OTU level. Trees 4, 5, and 6 were sprayed with streptomycin on 29 and 30 April 2010. (a) Rarefied Faith’s phylogenetic diversity of microorganisms. There were 10 resamples at a depth of 1,531 sequences for each tree at each time point. Letters indicate significant differences in phylogenetic diversity across days, assessed by analysis of variance (F = 101.56, 4 degrees of freedom [df], P < 0.001) and post hoc testing with Tukey’s HSD test (P < 0.05). (b) Variability in community structure (assessed by analysis of beta dispersion, a metric of variability). Though modest differences were detected (multivariate homogeneity of group dispersions; F = 2.34, 4 df, P = 0.08), a post hoc test revealed that only 27 and 29 April were different (Tukey’s HSD test; P = 0.09).

Mentions: Analysis of temporal patterns showed that phylogenetic diversity increased between 27 and 29 April and then stabilized (Fig. 3a). Additionally, variability in community structure was high before flowers opened, decreased when flowers opened, and then increased to prebloom levels through the rest of the life of the flower (Fig. 3b), suggesting that open flowers may have a more narrowly defined community than closed flowers. Though there were differences between some time points, there were no general temporal trends in evenness or richness (see the results in Text S1 in the supplemental material). We also detected differences in community structure across time points, but there was no effect of streptomycin treatment or of a time-treatment interaction (Table S1). Together, these results and others (Fig. S2) suggest that changes in apple flower microbial communities are patterned over time.


Unexpected diversity during community succession in the apple flower microbiome.

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

Temporal trends in the apple flower microbiome. For each time point, n = 6 (1 sample of DNA extracted in bulk from 15 flowers from each of six trees). The inner-quartile ranges are shown by the box boundaries, nonoutlier extremes are shown by the whiskers, the median is shown by the thick middle line, and outliers are shown by the outliers’ black points. Statistics were summarized across each of six trees sampled at each time point, and the communities were analyzed at the 97% OTU level. Trees 4, 5, and 6 were sprayed with streptomycin on 29 and 30 April 2010. (a) Rarefied Faith’s phylogenetic diversity of microorganisms. There were 10 resamples at a depth of 1,531 sequences for each tree at each time point. Letters indicate significant differences in phylogenetic diversity across days, assessed by analysis of variance (F = 101.56, 4 degrees of freedom [df], P < 0.001) and post hoc testing with Tukey’s HSD test (P < 0.05). (b) Variability in community structure (assessed by analysis of beta dispersion, a metric of variability). Though modest differences were detected (multivariate homogeneity of group dispersions; F = 2.34, 4 df, P = 0.08), a post hoc test revealed that only 27 and 29 April were different (Tukey’s HSD test; P = 0.09).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig3: Temporal trends in the apple flower microbiome. For each time point, n = 6 (1 sample of DNA extracted in bulk from 15 flowers from each of six trees). The inner-quartile ranges are shown by the box boundaries, nonoutlier extremes are shown by the whiskers, the median is shown by the thick middle line, and outliers are shown by the outliers’ black points. Statistics were summarized across each of six trees sampled at each time point, and the communities were analyzed at the 97% OTU level. Trees 4, 5, and 6 were sprayed with streptomycin on 29 and 30 April 2010. (a) Rarefied Faith’s phylogenetic diversity of microorganisms. There were 10 resamples at a depth of 1,531 sequences for each tree at each time point. Letters indicate significant differences in phylogenetic diversity across days, assessed by analysis of variance (F = 101.56, 4 degrees of freedom [df], P < 0.001) and post hoc testing with Tukey’s HSD test (P < 0.05). (b) Variability in community structure (assessed by analysis of beta dispersion, a metric of variability). Though modest differences were detected (multivariate homogeneity of group dispersions; F = 2.34, 4 df, P = 0.08), a post hoc test revealed that only 27 and 29 April were different (Tukey’s HSD test; P = 0.09).
Mentions: Analysis of temporal patterns showed that phylogenetic diversity increased between 27 and 29 April and then stabilized (Fig. 3a). Additionally, variability in community structure was high before flowers opened, decreased when flowers opened, and then increased to prebloom levels through the rest of the life of the flower (Fig. 3b), suggesting that open flowers may have a more narrowly defined community than closed flowers. Though there were differences between some time points, there were no general temporal trends in evenness or richness (see the results in Text S1 in the supplemental material). We also detected differences in community structure across time points, but there was no effect of streptomycin treatment or of a time-treatment interaction (Table S1). Together, these results and others (Fig. S2) suggest that changes in apple flower microbial communities are patterned over time.

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