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Nectar sugars and bird visitation define a floral niche for basidiomycetous yeast on the Canary Islands.

Mittelbach M, Yurkov AM, Nocentini D, Nepi M, Weigend M, Begerow D - BMC Ecol. (2015)

Bottom Line: Our results show these basidiomycetes are significantly associated with ornithophilous flowers.There are two conclusions from this study: (i) a shift of floral visitors towards ornithophily alters the likelihood of yeast inoculation in flowers, and (ii) low concentrated hexose-dominant nectar promotes colonization of flowers by basidiomycetes.This challenges the current understanding that nectar is an ecological niche solely occupied by ascomycetous yeasts.

View Article: PubMed Central - PubMed

Affiliation: Department of Geobotany, - LS Evolution & Biodiversity of Plants, Ruhr-University Bochum, ND 1/150 / Universitaetsstr, 150, Bochum, 44780, Germany. moritz.mittelbach@rub.de.

ABSTRACT

Background: Studies on the diversity of yeasts in floral nectar were first carried out in the late 19th century. A narrow group of fermenting, osmophilous ascomycetes were regarded as exclusive specialists able to populate this unique and species poor environment. More recently, it became apparent that microorganisms might play an important role in the process of plant pollination. Despite the importance of these nectar dwelling yeasts, knowledge of the factors that drive their diversity and species composition is scarce.

Results: In this study, we linked the frequencies of yeast species in floral nectars from various host plants on the Canary Islands to nectar traits and flower visitors. We estimated the structuring impact of pollination syndromes (nectar volume, sugar concentration and sugar composition) on yeast diversity.The observed total yeast diversity was consistent with former studies, however, the present survey yielded additional basidiomycetous yeasts in unexpectedly high numbers. Our results show these basidiomycetes are significantly associated with ornithophilous flowers. Specialized ascomycetes inhabit sucrose-dominant nectars, but are surprisingly rare in nectar dominated by monosaccharides.

Conclusions: There are two conclusions from this study: (i) a shift of floral visitors towards ornithophily alters the likelihood of yeast inoculation in flowers, and (ii) low concentrated hexose-dominant nectar promotes colonization of flowers by basidiomycetes. In the studied floral system, basidiomycete yeasts are acknowledged as regular members of nectar. This challenges the current understanding that nectar is an ecological niche solely occupied by ascomycetous yeasts.

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Growth curves of selected strains. Growth curves of selected strains in artificial nectar medium with 40% sugar concentration measured as OD 600. Shaded areas correspond to standard errors calculated of 16 replicates.
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Fig5: Growth curves of selected strains. Growth curves of selected strains in artificial nectar medium with 40% sugar concentration measured as OD 600. Shaded areas correspond to standard errors calculated of 16 replicates.

Mentions: (i) Among other natural yeast harboring substrates, such as plant surfaces, fruits, and soils [26,27,49], nectar habitats stand out by high sugar concentrations, microaerophilic conditions, low nitrogen levels, and the widespread presence of anti-microbial compounds [50]. As has been shown by Peay et al. [29], these environmental conditions may regulate the growth of nectar dwelling microorganisms, giving nectar a filtering property for inoculated colonizers. Our results supported this hypothesis, as increased sugar concentrations favored the growth of only a few highly specialized ascomycetes (Figure 4). We also isolated strains of Cr. carnescens and Cys. capitatum from sugar rich nectars (Additional file 1) and showed positive growth in kinetic laboratory experiments with up to 40% sugar, which indicated their ability to grow in nectars of all studied host plants (Figure 5). Together with our results that basidiomycetous yeasts are significantly more successful in colonizing hexose dominant nectars (Figure 3), we conclude that sugar concentration alone cannot explain the composition of yeast communities in floral nectars. Additional factors, such as sugar composition (Figure 2) and a prolonged flower lifetime might be important selective filters of yeast communities in the sampled ornithophilous host plants. The latter should favor the establishment of basidiomycetes in nectar, accounting for their slower growth and extended lag phase in kinetic growth experiments in comparison to tested ascomycetous specialists (Figure 5).Figure 5


Nectar sugars and bird visitation define a floral niche for basidiomycetous yeast on the Canary Islands.

Mittelbach M, Yurkov AM, Nocentini D, Nepi M, Weigend M, Begerow D - BMC Ecol. (2015)

Growth curves of selected strains. Growth curves of selected strains in artificial nectar medium with 40% sugar concentration measured as OD 600. Shaded areas correspond to standard errors calculated of 16 replicates.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4318194&req=5

Fig5: Growth curves of selected strains. Growth curves of selected strains in artificial nectar medium with 40% sugar concentration measured as OD 600. Shaded areas correspond to standard errors calculated of 16 replicates.
Mentions: (i) Among other natural yeast harboring substrates, such as plant surfaces, fruits, and soils [26,27,49], nectar habitats stand out by high sugar concentrations, microaerophilic conditions, low nitrogen levels, and the widespread presence of anti-microbial compounds [50]. As has been shown by Peay et al. [29], these environmental conditions may regulate the growth of nectar dwelling microorganisms, giving nectar a filtering property for inoculated colonizers. Our results supported this hypothesis, as increased sugar concentrations favored the growth of only a few highly specialized ascomycetes (Figure 4). We also isolated strains of Cr. carnescens and Cys. capitatum from sugar rich nectars (Additional file 1) and showed positive growth in kinetic laboratory experiments with up to 40% sugar, which indicated their ability to grow in nectars of all studied host plants (Figure 5). Together with our results that basidiomycetous yeasts are significantly more successful in colonizing hexose dominant nectars (Figure 3), we conclude that sugar concentration alone cannot explain the composition of yeast communities in floral nectars. Additional factors, such as sugar composition (Figure 2) and a prolonged flower lifetime might be important selective filters of yeast communities in the sampled ornithophilous host plants. The latter should favor the establishment of basidiomycetes in nectar, accounting for their slower growth and extended lag phase in kinetic growth experiments in comparison to tested ascomycetous specialists (Figure 5).Figure 5

Bottom Line: Our results show these basidiomycetes are significantly associated with ornithophilous flowers.There are two conclusions from this study: (i) a shift of floral visitors towards ornithophily alters the likelihood of yeast inoculation in flowers, and (ii) low concentrated hexose-dominant nectar promotes colonization of flowers by basidiomycetes.This challenges the current understanding that nectar is an ecological niche solely occupied by ascomycetous yeasts.

View Article: PubMed Central - PubMed

Affiliation: Department of Geobotany, - LS Evolution & Biodiversity of Plants, Ruhr-University Bochum, ND 1/150 / Universitaetsstr, 150, Bochum, 44780, Germany. moritz.mittelbach@rub.de.

ABSTRACT

Background: Studies on the diversity of yeasts in floral nectar were first carried out in the late 19th century. A narrow group of fermenting, osmophilous ascomycetes were regarded as exclusive specialists able to populate this unique and species poor environment. More recently, it became apparent that microorganisms might play an important role in the process of plant pollination. Despite the importance of these nectar dwelling yeasts, knowledge of the factors that drive their diversity and species composition is scarce.

Results: In this study, we linked the frequencies of yeast species in floral nectars from various host plants on the Canary Islands to nectar traits and flower visitors. We estimated the structuring impact of pollination syndromes (nectar volume, sugar concentration and sugar composition) on yeast diversity.The observed total yeast diversity was consistent with former studies, however, the present survey yielded additional basidiomycetous yeasts in unexpectedly high numbers. Our results show these basidiomycetes are significantly associated with ornithophilous flowers. Specialized ascomycetes inhabit sucrose-dominant nectars, but are surprisingly rare in nectar dominated by monosaccharides.

Conclusions: There are two conclusions from this study: (i) a shift of floral visitors towards ornithophily alters the likelihood of yeast inoculation in flowers, and (ii) low concentrated hexose-dominant nectar promotes colonization of flowers by basidiomycetes. In the studied floral system, basidiomycete yeasts are acknowledged as regular members of nectar. This challenges the current understanding that nectar is an ecological niche solely occupied by ascomycetous yeasts.

Show MeSH