A mutualistic bacterium rescues a green alga from an antagonist

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 <i>Pseudomonas protegens</i> acts algicidal on the microalga <i>Chlamydomonas reinhardtii.</i> It secretes a cyclic lipopeptide and a polyyne that deflagellate, blind, and lyse the algae [P. Aiyar <i>et al.</i>, <i>Nat. Commun.</i> <b>8</b>, 1756 (2017) and V. Hotter <i>et al.</i>, <i>Proc. Natl. Acad. Sci. U.S.A.</i> <b>118</b>, e2107695118 (2021)]. Here, we report about the bacterium <i>Mycetocola lacteus,</i> which establishes a mutualistic relationship with <i>C. reinhardtii</i> and acts as a helper. While <i>M. lacteus</i> enhances algal growth, it receives methionine as needed organic sulfur and the vitamins B₁, B₃, and B₅ from the algae. In tripartite cultures with the alga and the antagonistic bacterium <i>P. protegens</i>, <i>M. lacteus</i> aids the algae in surviving the bacterial attack. By combining synthetic natural product chemistry with high-resolution mass spectrometry and an algal Ca²⁺ reporter line, we found that <i>M. lacteus</i> 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 Ca²⁺ 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 <i>Pseudomonas</i> and <i>Mycetocola</i> also act antagonistically against <i>C. reinhardtii</i> or as helper bacteria in tripartite cultures.