Unveiling Crocosphaera responses to phosphorus depletion: insights from genome analysis and functional characterization

Unicellular, nitrogen-fixing cyanobacteria (UCYN) thrive and support primary production in oligotrophic oceans, playing a significant role in the marine nitrogen cycle. Crocosphaera sp, a model for studying marine nitrogen fixation, is adapted to low phosphate (Pi) conditions. Yet, how Crocosphaera copes with Pi depletion is rather poorly understood. We present genomics analysis of Pi stress-responsive genes in this genus, encompassing six C. watsonii genomes and two strains isolated in coastal environments, C. subtropica and C. chwakensis. We identified genes involved in Pi signaling, uptake, and dissolved organic phosphorus (DOP) hydrolysis. Results showed different genetic potentials to cope with Pi scarcity between the Crocosphaera strains. Physiological monitoring of cultures of C. watsonii WH8501 exposed to Pi depletion highlighted a capacity to divide several times and survive for a few more days, albeit with a skewed C:N:P stoichiometry. Upon addition of DOP, cultures efficiently recovered to a growth rate and cell composition equivalent to those observed under favorable conditions. The concomitant transcription analysis revealed diel expression patterns of Pi-related genes and endogenous clock genes, suggesting a possible circadian regulation. Our data deepen our understanding of the growth strategies Crocosphaera employs in Pi-limited environments, offering broader insights into microbial resilience in marine ecosystems.