Nectar microbial community assembly and plant-pollinator mutualism
An increasing number of studies suggest that microorganisms found in floral nectar can affect plant fitness by altering nectar chemistry and, consequently, the attractiveness of flowers to pollinators. It has also been shown that nectar microbes rely on pollinators for flower-to-flower dispersal. These studies point to the potential for significant feedback among microbes, animals, and plants. However, it is not well understood how microbial species may vary in their effects on plants and animals or how they may develop and function as multi-species communities, despite ample evidence for the functional diversity of microbial species and the importance of species interactions in structuring microbial communities. We address these questions by synthesizing four lines of evidence from several field and laboratory experiments we recently conducted.
First, experimental inoculation of hummingbird-pollinated Mimulus aurantiacus flowers with nectar microbes in the field indicated that flowers were pollinated less frequently and yielded fewer seeds when colonized by the common bacterium Gluconobacter sp., compared with no microbial inoculation control. In contrast, the common yeast, Metchnikowia reukaufii, had no detectable effect on pollination or seed production. Second, field experiments using real and synthetic nectar inoculated with different microbial species indicated that two taxonomically disparate pollinators, the hummingbird Calypte anna and the honeybee Apis mellifera, were both less likely to consume nectar colonized by bacterial species, including Asaia astilbes, Erwinia tasmaniensis, Gluconobacter sp., and Lactobacillus kunkeei, compared with nectar colonized by the yeast M. reukaufii. Third, laboratory experiments using several species indicated that bacterial and yeast species had differential effects on, and response to, a variety of chemical properties of nectar, including pH and the composition and concentration of sugars, amino acids, and secondary compounds. Fourth, another set of laboratory experiments, with the yeasts M. reukaufii and Starmerella bombicola and the bacteria Gluconobacter sp. and A. astilbes, revealed that yeasts and bacteria could affect each other, often resulting in competitive exclusion, and that whether yeasts or bacteria dominated could depend strongly on the order in which they colonized nectar. Taken together, these findings suggest that the assembly history of microbial communities shapes microbial species composition in nectar via changes in nectar chemistry and that these microbial and chemical changes in turn can affect pollinator behavior and plant fitness. Overall, our work suggests that it may not be possible to explain the impacts of floral microbes on plants and animals without understanding how microbial species assemble into communities in flowers.