Unveiling Crocosphaera Responses to Phosphorus Depletion: Insights From Genome Analysis and Functional Characterization

Abstract

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 organism for studying marine nitrogen fixation, is adapted to low phosphate (P_i) concentrations. Yet, how Crocosphaera copes with P_i depletion is rather poorly understood. We present a genomics analysis of P_i stress-responsive genes in this genus, encompassing six C. watsonii and two strains isolated in coastal environments, C. subtropica and C. chwakensis. We identified genes involved in P_i signalling and uptake, and dissolved organic phosphorus (DOP) hydrolysis. Results showed different genetic potentials to cope with P_i scarcity between the Crocosphaera strains. Physiological monitoring of cultures of C. watsonii WH8501 exposed to P_i depletion highlighted a capacity to survive for at least nine 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 favourable conditions. The concomitant transcription analysis revealed diel expression patterns of P_i-related genes and endogenous clock genes, suggesting a possible circadian regulation. Our data deepen our understanding of the growth strategies Crocosphaera employs in P_i-limited environments, offering broader insights into microbial resilience in marine ecosystems.