Symbiont selection via alcohol benefits fungus farming by ambrosia beetles

Autor: Christopher M. Ranger, Peter B. Schultz, J. Philipp Benz, Satyaki Ghosh, Peter H. W. Biedermann, Vipaporn Phuntumart, Jenny Barnett, Debra E. Palmquist, Gayathri Udayangika Beligala, Robert Mueller, M.E. Reding
Rok vydání: 2018
Předmět:
Zdroj: Proceedings of the National Academy of Sciences of the United States of America
Popis: Significance Ambrosia beetles are among the true fungus-farming insects and cultivate fungal gardens on which the larvae and adults feed. After invading new habitats, some species destructively attack living or weakened trees growing in managed and unmanaged settings. Ambrosia beetles adapted to weakened trees tunnel into stem tissues containing ethanol to farm their symbiotic fungi, even though ethanol is a potent antimicrobial agent that inhibits the growth of various fungi, yeasts, and bacteria. Here we demonstrate that ambrosia beetles rely on ethanol for host tree colonization because it promotes the growth of their fungal gardens while inhibiting the growth of “weedy” fungal competitors. We propose that ambrosia beetles use ethanol to optimize their food production.
Animal–microbe mutualisms are typically maintained by vertical symbiont transmission or partner choice. A third mechanism, screening of high-quality symbionts, has been predicted in theory, but empirical examples are rare. Here we demonstrate that ambrosia beetles rely on ethanol within host trees for promoting gardens of their fungal symbiont and producing offspring. Ethanol has long been known as the main attractant for many of these fungus-farming beetles as they select host trees in which they excavate tunnels and cultivate fungal gardens. More than 300 attacks by Xylosandrus germanus and other species were triggered by baiting trees with ethanol lures, but none of the foundresses established fungal gardens or produced broods unless tree tissues contained in vivo ethanol resulting from irrigation with ethanol solutions. More X. germanus brood were also produced in a rearing substrate containing ethanol. These benefits are a result of increased food supply via the positive effects of ethanol on food-fungus biomass. Selected Ambrosiella and Raffaelea fungal isolates from ethanol-responsive ambrosia beetles profited directly and indirectly by (i) a higher biomass on medium containing ethanol, (ii) strong alcohol dehydrogenase enzymatic activity, and (iii) a competitive advantage over weedy fungal garden competitors (Aspergillus, Penicillium) that are inhibited by ethanol. As ambrosia fungi both detoxify and produce ethanol, they may maintain the selectivity of their alcohol-rich habitat for their own purpose and that of other ethanol-resistant/producing microbes. This resembles biological screening of beneficial symbionts and a potentially widespread, unstudied benefit of alcohol-producing symbionts (e.g., yeasts) in other microbial symbioses.
Databáze: OpenAIRE