The yeast spore wall enables spores to survive passage through the digestive tract of Drosophila

Abstract

In nature, yeasts are subject to predation by flies of the genus Drosophila. In response to nutritional starvation Saccharomyces cerevisiae differentiates into a dormant cell type, termed a spore, which is resistant to many types of environmental stress. The stress resistance of the spore is due primarily to a spore wall that is more elaborate than the vegetative cell wall. We report here that S. cerevisiae spores survive passage through the gut of Drosophila melanogaster. Constituents of the spore wall that distinguish it from the vegetative cell wall are necessary for this resistance. Ascospores of the distantly related yeast Schizosaccharomyces pombe also display resistance to digestion by D. melanogaster. These results suggest that the primary function of the yeast ascospore is as a cell type specialized for dispersion by insect vectors.

Figure 1. Relative survival of stationary phase cells, log phase cells and spores to different stresses.

The survival of vegetative cells from a saturated culture (Sat), a log phase culture (Log), or spores (Spo) after exposure to various stresses was measured as described in the Methods. For each condition, at least three independent experiments were performed and the average percent survival determined. For the graph, the survival rate of spores was defined as 1 and the relative survival of the vegetative cultures is shown. Thin lines represent the range of relative survival. The average percent survivals of spores under each condition were: 40% dextrose, 60%; β-glucanase, 244%; Acetic acid, 54%; NaOH, 23%; Ether 52%; Freeze/Thaw 94%; 2M Sorbitol, 76%; 42°C, 73%; 5M NaCl, 51%.

Figure 2. Spores are intact in Drosophila frass.

Vegetative cells or spores of strain AN390 were fed to Drosophila and the frass was analyzed by DIC and fluorescence microscopy. A) DIC image of vegetative cells before ingestion. B) Fluorescence image of cells in A. C) DIC image of a flyspeck from Drosophila fed vegetative cells. Arrow indicates an intact vegetative cell. D) Fluorescence image of cells in C. E) DIC image of spores before ingestion. F) Fluorescence image of spores in E. G) DIC image of a flyspeck from Drosophila fed spores. H) Fluorescence image of cells in G. Scale bar = 5 microns.

Figure 3. Spores with defective spore walls display reduced survival in frass.

Spores mutant for dit1, mum3, or osw1 were fed to Drosophila and the frass was analyzed by DIC and fluorescence microscopy. A) DIC image of dit1 spores before ingestion. B) DIC image of dit1 spores in frass. Arrow indicates an intact spore. Arrowhead indicates a lysed spore. C) Fluorescence image of spores in A. D) Fluorescence image of spores in B. E) DIC image of mum3 spores before ingestion. F) DIC image of mum3 spores after ingestion. G) DIC image of osw1 spores before ingestion. H) DIC image of osw1 spores in frass.

Figure 4. S. pombe spores display increased resistance to passage through Drosophila.

Vegetative or sporulated cells of strain YDM124 were fed to Drosophila and flyspecks were analyzed by light microscopy. A) Vegetative cells before ingestion. B) Vegetative cells in frass. Arrow indicates an intact cell. C) Spores before ingestion. D) Spores in frass. Arrow indicates an intact spore. Arrowhead indicates a lysed spore.