Lichen-like association of Chlamydomonas reinhardtii and Aspergillus nidulans protects algal cells from bacteria

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.

Species in lichen-forming fungi: balancing between conceptual and practical considerations, and between phenotype and phylogenomics

“…Given extant lichens, one could specify the fungal component as a member of the kingdom Fungi, but what would a theoretical association involving a member of the Oomycota then constitute and how could one exclude that associations with other fungal-like organisms might exist or might have existed in the past? Associations with photosynthetic algae have also been formed by fungal-like bacteria (Actinomycetes) and by fungi otherwise not forming lichens, such as in the genus Aspergillus, under laboratory conditions (Lazo 1966;Lawrey 1984;Zvyagintsev et al 2010;Lücking and Nelsen 2018;Krespach et al 2020). Since photobionts of lichens represent two domains (including Bacteria) and three kingdoms, there would be no logical reason to restrict mycobionts to a single domain (excluding Bacteria) and kingdom.…”

Deciphering microbiome impacts on fungal-microalgal interaction in a marine environment using metabolomics

“…In this specific association, the two species were forced, under specific conditions, to mutually support each other's growth. In a very recent study, during the tripartite interaction between C. reinhardtii, Aspergillus nidulans and Streptomyces iranensis, the fungal species was demonstrated to physically defend the microalgae from bacterial algicide compound azalomycin F by forming a protective lipid coat as observed by microscopy [79].…”

A polyyne toxin produced by an antagonistic bacterium blinds and lyses a green microalga

“…However, C. reinhardtii can also be prone to be attacked by antagonistic bacteria. For example, the soil bacterium Streptomyces iranensis releases the algicide azalomycin F, which is toxic for C. reinhardtii unless the alga protects itself among the mycelia of the fungus Aspergillus nidulans (15). In a previous study, we showed that another soil bacterium, Pseudomonas protegens Pf-5, known to produce a wide variety of secondary metabolites (16), can inhibit the growth of C. reinhardtii (17).…”