Multiomics dissection of the CO2-dependent fast growth of Picochlorum celeri

Abstract

With a sub-3-micrometer cell and a 27-Mbp diploid genome, the small but mighty Picochlorum celeri doubles within three hours and exceeds 30 g m-2 d-1 outdoors with CO2 supplied. In climate-simulating photobioreactors, productivity declined from 39 g m-2 d-1 under 2.25% CO2 to near zero in air and resumed within hours of CO2 restoration with photosystem II photochemistry largely retained. We profiled the transcriptome, proteome, phosphoproteome, ubiquitinome, acetylome, metabolome and lipidome, including the first site-resolved green-algal ubiquitinome. In air, the Rubisco large subunit tripled to 7.6% of protein while its two small-subunit isoforms, 70% identical, exchanged near-reciprocally, a novel CO2-dependent switch that we propose retunes Rubisco to low CO2. Photorespiratory enzymes increased in abundance whereas proteins involved in external nitrogen assimilation decreased, consistent with increased reliance on internal nitrogen recycling as carbon fixation became limiting. Transcript and protein responses were nearly uncoupled, with cytosolic ribosomal proteins declining despite increased transcripts and plastid ribosomal proteins spared. Phosphorylation was extensively remodeled, as were the lysine modifications ubiquitination, acetylation and CO2-dependent carbamylation, where a CO2-competition assay identified 86 bicarbonate-protected lysines, including RbcL K252. CO2 limitation therefore imposes a reversible growth arrest that reduces cytosolic translational investment while preserving photosynthetic capacity for rapid recovery.