Cyanophycin accumulated under nitrogen-fluctuating and high-nitrogen conditions facilitates the persistent dominance and blooms of Raphidiopsis raciborskii in tropical waters.

Nutrient storage is considered a critical strategy for algal species to adapt to a fluctuating nutrient supply. Luxury phosphorus (P) uptake into storage of polyphosphate extends the duration of cyanobacterial dominance and their blooms under P deficiency. However, it is unclear whether nitrogen (N) storage in the form of cyanophycin supports persistent cyanobacterial dominance or blooms in the tropics where N deficiency commonly occurs in summer. In this study, we examined genes for cyanophycin synthesis and degradation in Raphidiopsis raciborskii, a widespread and dominant cyanobacterium in tropical waters; and detected the cyanophycin accumulation under fluctuating N concentrations and its ecological role in the population dynamics of the species. The genes for cyanophycin synthesis (cphA) and degradation (cphB) were highly conserved in 21 out of 23 Raphidiopsis strains. This suggested that the synthesis and degradation of cyanophycin are evolutionarily conserved to support the proliferation of R. raciborskii in N-fluctuating and/or deficient conditions. Isotope N-NaNO labeling experiments showed that R. raciborskii QDH7 always commenced to synthesize and accumulate cyanophycin under fluctuating N conditions, regardless of whether exogenous N was deficient. When the NO-N concentration exceeded 1.2 mg L, R. raciborskii synthesized cyanophycin primarily through uptake of N-NaNO. However, when the NO-N concentration was below 1.0 mg L, cyanophycin-based N was derived from unlabeled N, as evidenced by increased dinitrogenase activity. Cells grown under NO-N < 1.0 mg L had lower cyanophycin accumulation rates than cells grown under NO-N > 1.2 mg L. Our field investigation in a large tropical reservoir underscored the association between cyanophycin content and the population dynamics of R. raciborskii. The cyanophycin content was high in N-sufficient (NO-N > 0.45 mg L) periods, and decreased in N-deficient summer. In summer, R. raciborskii sustained a relatively high biomass and produced few heterocysts (< 1%). These findings indicated that cyanophycin-released N, rather than fixed N, supported persistent R. raciborskii blooms in N-deficient seasons. Our study suggests that the highly adaptive strategy in a N-fixing cyanobacterial species makes mitigating its bloom more difficult than previously assumed.