Fruiting bodies of the social amoeba Dictyostelium discoideum increase spore transport by Drosophila

Abstract

Background: Many microbial phenotypes are the product of cooperative interactions among cells, but their putative fitness benefits are often not well understood. In the cellular slime mold Dictyostelium discoideum, unicellular amoebae aggregate when starved and form multicellular fruiting bodies in which stress-resistant spores are held aloft by dead stalk cells. Fruiting bodies are thought to be adaptations for dispersing spores to new feeding sites, but this has not been directly tested. Here we experimentally test whether fruiting bodies increase the rate at which spores are acquired by passing invertebrates.

Results: Drosophila melanogaster accumulate spores on their surfaces more quickly when exposed to intact fruiting bodies than when exposed to fruiting bodies physically disrupted to dislodge spore masses from stalks. Flies also ingest and excrete spores that still express a red fluorescent protein marker.

Conclusions: Multicellular fruiting bodies created by D. discoideum increase the likelihood that invertebrates acquire spores that can then be transported to new feeding sites. These results thus support the long-hypothesized dispersal benefits of altruism in a model system for microbial cooperation.

Figure 1

Fruiting bodies created by social amoebae increase spore dispersal by arthropods. (A) Dispersal assay. Amoebae created fruiting bodies on agar in the bottom of a conical tube. We disrupted fruiting bodies in some tubes by banging them several times against a hard surface, dislodging spore masses and causing fruiting bodies to fall over. We then turned tubes sideways and introduced fruit flies. At various times we sampled tubes and counted spores recovered from washed flies. (B) Flies pick up spores more readily from intact fruiting bodies. Data show mean ± SEM of 3–4 independent experimental replicates.

Figure 2

Location of carried spores. (A-C) Spores accumulated on D. melanogaster legs, wings, eyes, and mouthparts. Flies also ingested (B) and excreted (C) spores without degrading fluorescence. (D) Fly not exposed to spores. Images show composite of reflected light and red fluorescence.