Abstract
Organismal interactions within microbial consortia and their responses to harmful intruders remain largely understudied. An important step toward the goal of understanding functional ecological interactions and their evolutionary selection is the study of increasingly complex microbial interaction systems. Here, we discovered a tripartite biosystem consisting of the fungus Aspergillus nidulans, the unicellular green alga Chlamydomonas reinhardtii, and the algicidal bacterium Streptomyces iranensis. Genetic analyses and MALDI-IMS demonstrate that the bacterium secretes the algicidal compound azalomycin F upon contact with C. reinhardtii. In co-culture, A. nidulans attracts the motile alga C. reinhardtii, which becomes embedded and surrounded by fungal mycelium and is shielded from the algicide. The filamentous fungus Sordaria macrospora was susceptible to azalomycin F and failed to protect C. reinhardtii despite chemotactically attracting the alga. Because S. macrospora was susceptible to azalomycin F, this data imply that for protection the fungus needs to be resistant. Formation of the lichen-like association between C. reinhardtii and A. nidulans increased algal growth. The protection depends on the increased amounts of membrane lipids provided by resistant fungi, thereby generating a protective shelter against the bacterial toxin. Our findings reveal a strategy whereby algae survive lethal environmental algicides through cooperation with fungi.
Highlights
Algae and fungi have coexisted and coevolved for at least 400 million years, as deduced from fossil records showing macroalgae parasitized by fungi [1], as well as lichens [2, 3]
We have found a tripartite interaction of the model green alga C. reinhardtii with the established bipartite A. nidulans-S. iranensis co-culture system [17]. We found that both partners have distinct effects on the alga: (i) the bacterium kills the alga using the natural product azalomycin F, (ii) the alga is protected by fungi resistant against azalomycin F like A. nidulans, and (iii) the presence of A. nidulans increases the growth rate and overall biomass of C. reinhardtii
A. nidulans and the green alga C. reinhardtii quickly assemble in co-culture to form an algal–fungal association [19]
Summary
Algae and fungi have coexisted and coevolved for at least 400 million years, as deduced from fossil records showing macroalgae parasitized by fungi [1], as well as lichens [2, 3]. Tight associations between algae and fungi, in particular in lichens, provide examples of mutualism that has been maintained over hundreds of millions of years up to the present [4]. Microorganisms are often subject to rapidly changing biotic and abiotic conditions in their natural habitats. To cope with these environmental changes, they often produce natural products that are low molecular mass metabolites [7, 8]. They are often dispensable for growth, produced at a certain stage
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