Marine picocyanobacteria are among the most abundant primary producers in the oceans, forming the foundation of marine food webs. They play a crucial role in global biogeochemical cycles by fixing carbon and producing oxygen through photosynthesis. Recent genomic and proteomic evidence suggests that these organisms possess mixotrophic capabilities, enabling the uptake and utilisation of both inorganic and organic compounds. This challenges the long-held view of picocyanobacteria as obligate photoautotrophs. Their streamlined genomes encode diverse predicted nutrient uptake systems for both inorganic and organic nutrients. Most nutrient uptake in picocyanobacteria is mediated by ATP-binding cassette (ABC) transporters, which are associated with substrate-binding proteins (SBPs) to confer substrate specificity. Therefore, the SBPs can be used as proxies to understand the functional role of the ABC uptake family in picocyanobacterial nutrient acquisition.
In this study, we identify and characterise a predicted nitrate-binding protein in Synechococcus sp. CC9311 exhibits an unexpected and specific affinity for guanidine, a nitrogenous chaotropic compound. Contrary to predictions, this protein shows no detectable affinity for any other nitrogen source, including amino acids, but binds strongly to guanidine and is hereafter referred to as the guanidine-binding protein (CC9311_GBP). Physiological assays revealed that Synechococcus CC9311 cells supplemented with guanidine showed reduced pigment degradation compared to nitrogen-starved controls, suggesting that guanidine may serve as an alternate nitrogen source. Genomic analysis further identified that Synechococcus CC9311 encodes agmatinase, a recently characterised guanidinase that converts guanidine into ammonia. Interestingly, genomic context analysis showed that the CC9311_GBP lacks adjacent ABC transporter components, unlike similar systems in other cyanobacterial strains. Our ongoing transcriptomic and proteomic studies aim to further investigate the metabolic role and transporter components of CC9311_GBP in Synechococcus CC9311.
This study identifies CC9311_GBP as a novel guanidine-binding protein, highlighting the importance of experimentally validating predicted gene functions. It provides new insight into nutrient acquisition and metabolic flexibility in marine picocyanobacteria. It underscores the need for broader exploration of SBPs to understand their roles in environmental adaptation and nitrogen utilisation.