Metamorphosis of a unicellular green alga in the presence of acetate and a spatially structured three-dimensional environment

Photosynthetic protists, named microalgae, are key players in global primary production. The green microalga Chlamydomonas reinhardtii is a well-studied model organism. In nature, it dwells in acetate-rich paddy rice soil, which is not mimicked by standard liquid laboratory conditions. Here, we maintained the algae in a liquid environment with spatially structured 3-D components (S3-D) and acetate recreating natural conditions. We perform transcriptome sequencing, immunoblotting, fluorescence and electron microscopy, and Raman microspectroscopy to characterize the algae in S3-D vs homogeneous conditions. The algae undergo a metamorphosis-like process when transitioned from homogeneous aquatic to a lifestyle simulating acetate-rich rice soil. These conditions result in reduced cell size and cilia length, an enlarged eyespot and many cells with double-layered cell walls. RNA-Seq reveals alterations in c. 2400 transcripts. Four key photoreceptors including CRY-DASH1 and phototropin governing plastid metabolism along with its eyespot are altered in their protein expression. Consequently, photosynthetic pigments, lipids and starch levels vary as do starch distribution patterns. Fitness against antagonistic bacteria is enhanced concurrently with the downregulation of an involved Ca²⁺ channel transcript. This study highlights the profound impact of S3-D initiating processes inaccessible under homogeneous laboratory conditions. Thus, overexpression lines for certain photoreceptors and starch are naturally created.