Tripartite synergy - Metabolic crosstalk between two bacterial mutualists and a marine microalga promotes algal fitness

Abstract

Marine microalgae form major parts of phytoplankton and are highly relevant for global CO2 fixation. Although microalgae have lived together with bacteria in the oceans for billions of years, these ecosystem-relevant interactions remain largely uncharacterized. Here, we have studied biotic interactions between two marine bacteria and a marine microalga. We show that an N2-fixing Vibrio provides ammonium for Chlamydomonas sp. and a Marinobacterium. Both microorganisms cannot survive in an ammonium-free environment. In exchange, the microalga promotes the growth of both bacteria, via secretion of heat-resistant metabolites in case of Marinobacterium. Reciprocally, the Marinobacterium releases heat-resistant metabolites that stimulate algal growth and increase its photosynthetic pigments, Photosystem II quantum yield, and starch accumulation. Electron microscopy reveals a strengthened starch sheath around the algal pyrenoid and indicates a modified periplasmic space for metabolic exchange. Our data highlight a tight synergy of a marine microbial trio promoting each others growth and algal fitness.