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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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Study design and flower anatomy. (A) Time course for sampling the apple microbiome. Fifteen pooled flowers from each of six Gala apple trees were collected at five time points over the life span of the flowers, for a total of 30 samples. Collection of phenologically matched flowers began before they opened and ended when petals fell. Arrows indicate streptomycin application. A precipitation event (1.30 cm) occurred on 30 April 2010. (B) Anatomy of a flower. All flower parts, including sepals, pistil, petals, and stamens, were included in the sampling. The current study provides a picture of the microbial communities that includes all of these flower compartments. (Reprinted from reference 81 with permission of the publisher.)
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fig1: Study design and flower anatomy. (A) Time course for sampling the apple microbiome. Fifteen pooled flowers from each of six Gala apple trees were collected at five time points over the life span of the flowers, for a total of 30 samples. Collection of phenologically matched flowers began before they opened and ended when petals fell. Arrows indicate streptomycin application. A precipitation event (1.30 cm) occurred on 30 April 2010. (B) Anatomy of a flower. All flower parts, including sepals, pistil, petals, and stamens, were included in the sampling. The current study provides a picture of the microbial communities that includes all of these flower compartments. (Reprinted from reference 81 with permission of the publisher.)

Mentions: Flowers provide ephemeral but nutrient-rich and protective habitats for microorganisms. In temperate climates, warm spring temperatures induce buds to open. Blooming exposes the male (stamen, including the anther and filament) (Fig. 1) and female (pistil, including the stigmata, style, and ovary) reproductive parts and inside surfaces of petals to the environment and microorganisms. Flower stigmas, in particular, exude sugars and amino acids that support a relatively large microbial load compared to that of other flower parts (8, 9). Previous studies have explored the culture-independent diversity of yeasts and fungi on flowers or in nectar (e.g., see references 10–12), culture-based diversity of bacteria on flowers (e.g., see references 9 and 12), and, quite recently, culture-independent diversity of bacteria in nectar (13), but none have considered the community diversity of flower-associated bacteria and archaea through time using culture-independent approaches.


Unexpected diversity during community succession in the apple flower microbiome.

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

Study design and flower anatomy. (A) Time course for sampling the apple microbiome. Fifteen pooled flowers from each of six Gala apple trees were collected at five time points over the life span of the flowers, for a total of 30 samples. Collection of phenologically matched flowers began before they opened and ended when petals fell. Arrows indicate streptomycin application. A precipitation event (1.30 cm) occurred on 30 April 2010. (B) Anatomy of a flower. All flower parts, including sepals, pistil, petals, and stamens, were included in the sampling. The current study provides a picture of the microbial communities that includes all of these flower compartments. (Reprinted from reference 81 with permission of the publisher.)
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig1: Study design and flower anatomy. (A) Time course for sampling the apple microbiome. Fifteen pooled flowers from each of six Gala apple trees were collected at five time points over the life span of the flowers, for a total of 30 samples. Collection of phenologically matched flowers began before they opened and ended when petals fell. Arrows indicate streptomycin application. A precipitation event (1.30 cm) occurred on 30 April 2010. (B) Anatomy of a flower. All flower parts, including sepals, pistil, petals, and stamens, were included in the sampling. The current study provides a picture of the microbial communities that includes all of these flower compartments. (Reprinted from reference 81 with permission of the publisher.)
Mentions: Flowers provide ephemeral but nutrient-rich and protective habitats for microorganisms. In temperate climates, warm spring temperatures induce buds to open. Blooming exposes the male (stamen, including the anther and filament) (Fig. 1) and female (pistil, including the stigmata, style, and ovary) reproductive parts and inside surfaces of petals to the environment and microorganisms. Flower stigmas, in particular, exude sugars and amino acids that support a relatively large microbial load compared to that of other flower parts (8, 9). Previous studies have explored the culture-independent diversity of yeasts and fungi on flowers or in nectar (e.g., see references 10–12), culture-based diversity of bacteria on flowers (e.g., see references 9 and 12), and, quite recently, culture-independent diversity of bacteria in nectar (13), but none have considered the community diversity of flower-associated bacteria and archaea through time using culture-independent approaches.

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