期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2021
卷号：118
期号：45
DOI：10.1073/pnas.2100892118
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
The physiological and ecological importance of natural products often remains obscured. Here, we report that
Streptomyces-derived marginolactones, a distinct group of soil-borne natural products, specifically trigger the formation of gloeocapsoids, previously undescribed protective aggregate structures produced by the unicellular green alga
Chlamydomonas reinhardtii. Gloeocapsoids are distinct palmelloids differing in their protective capability toward azalomycin F. The presence of marginolactone biosynthesis gene clusters in numerous streptomycetes, their ubiquity in soil, and our observation that three different members of this natural product group trigger the formation of gloeocapsoids suggest a cross-kingdom competition with ecological relevance. In the course of evolution, the polysaccharide matrix may have developed from a transient protective feature into the foundation of true multicellularity because of sustained marginolactone stress.
Photosynthetic microorganisms including the green alga
Chlamydomonas reinhardtii are essential to terrestrial habitats as they start the carbon cycle by conversion of CO
2 to energy-rich organic carbohydrates. Terrestrial habitats are densely populated, and hence, microbial interactions mediated by natural products are inevitable. We previously discovered such an interaction between
Streptomyces iranensis releasing the marginolactone azalomycin F in the presence of
C. reinhardtii. Whether the alga senses and reacts to azalomycin F remained unknown. Here, we report that sublethal concentrations of azalomycin F trigger the formation of a protective multicellular structure by
C. reinhardtii, which we named gloeocapsoid. Gloeocapsoids contain several cells which share multiple cell membranes and cell walls and are surrounded by a spacious matrix consisting of acidic polysaccharides. After azalomycin F removal, gloeocapsoid aggregates readily disassemble, and single cells are released. The presence of marginolactone biosynthesis gene clusters in numerous streptomycetes, their ubiquity in soil, and our observation that other marginolactones such as desertomycin A and monazomycin also trigger the formation of gloeocapsoids suggests a cross-kingdom competition with ecological relevance. Furthermore, gloeocapsoids allow for the survival of
C. reinhardtii at alkaline pH and otherwise lethal concentrations of azalomycin F. Their structure and polysaccharide matrix may be ancestral to the complex mucilage formed by multicellular members of the
Chlamydomonadales such as
Eudorina and
Volvox. Our finding suggests that multicellularity may have evolved to endure the presence of harmful competing bacteria. Additionally, it underlines the importance of natural products as microbial cues, which initiate interesting ecological scenarios of attack and counter defense.
