Nature's Most Fruitful Threesome: The Relationship between Yeasts, Insects, and Angiosperms

Abstract

The importance of insects for angiosperm pollination is widely recognized. In fact, approximately 90% of all plant species benefit from animal-mediated pollination. However, only recently, a third part player in this story has been properly acknowledged. Microorganisms inhabiting floral nectar, among which yeasts have a prominent role, can ferment glucose, fructose, sucrose, and/or other carbon sources in this habitat. As a result of their metabolism, nectar yeasts produce diverse volatile organic compounds (VOCs) and other valuable metabolites. Notably, some VOCs of yeast origin can influence insects' foraging behavior, e.g., by attracting them to flowers (although repelling effects have also been reported). Moreover, when insects feed on nectar, they also ingest yeast cells, which provide them with nutrients and protect them from pathogenic microorganisms. In return, insects serve yeasts as transportation and a safer habitat during winter when floral nectar is absent. From the plant's point of view, the result is flowers being pollinated. From humanity's perspective, this ecological relationship may also be highly profitable. Therefore, prospecting nectar-inhabiting yeasts for VOC production is of major biotechnological interest. Substances such as acetaldehyde, ethyl acetate, ethyl butyrate, and isobutanol have been reported in yeast volatomes, and they account for a global market of approximately USD 15 billion. In this scenario, the present review addresses the ecological, environmental, and biotechnological outlooks of this three-party mutualism, aiming to encourage researchers worldwide to dig into this field.

Keywords: angiosperms; bioprospection; floral nectar; insects; volatile organic compounds; yeasts.

Figure 1

Yeasts in flower nectaries ferment sugars, metabolize amino acids, and produce VOCs that might alter insects’ behavior. When these invertebrates feed on nectar, pollen is transported from anthers to the stigma (which may happen between different individual plants or between both parts in the same flower). Then, pollen germinates, and the pollen tube emanates, eventually allowing fertilization.

Figure 2

Pyruvate’s central role in VOC production from sugars occurring within the cells of Saccharomyces cerevisiae and other model yeasts. The hexoses glucose and fructose can be directly available in nectar or be generated from sucrose hydrolysis. Each mol of these hexoses is converted into two mols of pyruvate through the Embden–Meyerhof–Parnas (EMP) pathway, herein represented by a thick arrow. Pyruvate also works as a precursor of amino acids, such as valine, which can be found in nectar as well. VOCs are shown in bold italics. Acetaldehyde (underlined) can be either secreted as any other volatile compound or converted into different VOCs. Enzymes and coenzymes were omitted for the sake of simplification. Carbohydrate metabolism in Metschnikowia and other non-Saccharomyces yeasts prevalent in floral nectar remains greatly understudied. For further details, see the main text.