A mutualistic bacterium rescues a green alga from an antagonist

Author:

Carrasco Flores David1ORCID,Hotter Vivien1ORCID,Vuong Trang1ORCID,Hou Yu1ORCID,Bando Yuko2ORCID,Scherlach Kirstin3ORCID,Burgunter-Delamare Bertille1ORCID,Hermenau Ron3ORCID,Komor Anna J.3ORCID,Aiyar Prasad1ORCID,Rose Magdalena14ORCID,Sasso Severin14ORCID,Arndt Hans-Dieter25ORCID,Hertweck Christian356ORCID,Mittag Maria15ORCID

Affiliation:

1. Matthias Schleiden Institute of Genetics, Bioinformatics and Molecular Botany, General Botany, Friedrich Schiller University Jena, Jena 07743, Germany

2. Institute for Organic Chemistry and Macromolecular Chemistry, Organic Chemistry, Friedrich Schiller University Jena, Jena 07743, Germany

3. Department of Biomolecular Chemistry, Leibniz Institute for Natural Product Research and Infection Biology (Hans Knöll Institute), Jena 07745, Germany

4. Institute of Biology, Plant Physiology, Leipzig University, Leipzig 04103, Germany

5. Cluster of Excellence Balance of the Microverse, Friedrich Schiller University Jena, Jena 07743, Germany

6. Faculty of Biological Sciences, Friedrich Schiller University Jena, Jena 07743, Germany

Abstract

Photosynthetic protists, known as microalgae, are key contributors to primary production on Earth. Since early in evolution, they coexist with bacteria in nature, and their mode of interaction shapes ecosystems. We have recently shown that the bacterium Pseudomonas protegens acts algicidal on the microalga Chlamydomonas reinhardtii. It secretes a cyclic lipopeptide and a polyyne that deflagellate, blind, and lyse the algae [P. Aiyar et al. , Nat. Commun. 8 , 1756 (2017) and V. Hotter et al. , Proc. Natl. Acad. Sci. U.S.A. 118 , e2107695118 (2021)]. Here, we report about the bacterium Mycetocola lacteus, which establishes a mutualistic relationship with C. reinhardtii and acts as a helper. While M. lacteus enhances algal growth, it receives methionine as needed organic sulfur and the vitamins B 1 , B 3 , and B 5 from the algae. In tripartite cultures with the alga and the antagonistic bacterium P. protegens , M. lacteus aids the algae in surviving the bacterial attack. By combining synthetic natural product chemistry with high-resolution mass spectrometry and an algal Ca 2+ reporter line, we found that M. lacteus rescues the alga from the antagonistic bacterium by cleaving the ester bond of the cyclic lipopeptide involved. The resulting linearized seco acid does not trigger a cytosolic Ca 2+ homeostasis imbalance that leads to algal deflagellation. Thus, the algae remain motile, can swim away from the antagonistic bacteria and survive the attack. All three involved genera cooccur in nature. Remarkably, related species of Pseudomonas and Mycetocola also act antagonistically against C. reinhardtii or as helper bacteria in tripartite cultures.

Funder

Deutsche Forschungsgemeinschaft

Carl-Zeiss-Stiftung

International Leibniz Research School for Microbial and Biomolecular Interactions

Yoshida Scholarship Foundation

Publisher

Proceedings of the National Academy of Sciences

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