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Cyanobacteria are important primary producers, sources of secondary metabolites, and sentinels of environmental change in aquatic ecosystems – including large estuaries. Here, we newly investigated cyanobacterial diversity within the Albemarle Pamlico Sound System (APES) using (16S rRNA) gene amplicon sequencing analyses. Substantial cyanobacterial diversity including lineages lacking current isolates were recovered (46 genera, 17 potentially cyanotoxic), with oligohaline waters of the Albemarle Sound and its tributaries being notable regional hotspot for diversity. Salinity and temperature were influential drivers of cyanobacterial community composition. Picocyanobacteria (cells <3 µm in diameter) were abundant in amplicon sequence libraries (72% of cyanobacterial sequences) – especially populations withinSynechococcusSubClade 5.2. Picocyanobacteria along with picoeukaryotes were large contributors to total phytoplankton biomass comprising ~47% of chlorophyll a. Further, the picocyanobacterial generaSynechococcus,Cyanobium, andSynechocystis(55.4%, 14.8%, and 12.9% of cyanobacterial sequences, respectively) formed a core community spanning from freshwater regions (eastern AST, D949) to polyhaline environments (NRE100 downstream stations to PS5), suggesting resilience to significant salinity fluctuations and associated environmental changes. Amplicon sequence variant (ASV) and environmental data indicate the presence of several putative ecotypes, as well as distinct abundance patterns among closely related populations, highlighting substantial fitness variability among subspecies. Notably, potentially cyanotoxic genera,Synechocystis,Planktothrix,Plectonema, andDolichospermumwere the four more abundant detected in polyhaline APES regions, far beyond conspicuous freshwater sources. These findings reveal previously unrecognized potential sources of cyanotoxics in estuarine food webs and habitats, underscoring the ecological significance of cyanobacterial community dynamics across salinity gradients. 

ABSTRACT Vitamin B1 (thiamin) is a vital nutrient for most cells in nature, including marine plankton. Early and recent experiments show that B1 degradation products instead of B1 can support the growth of marine bacterioplankton and phytoplankton. However, the use and occurrence of some degradation products remains uninvestigated, namely N-formyl-4-amino-5-aminomethyl-2-methylpyrimidine (FAMP), which has been a focus of plant oxidative stress research. We investigated the relevance of FAMP in the ocean. Experiments and global ocean meta-omic data indicate that eukaryotic phytoplankton, including picoeukaryotes and harmful algal bloom species, use FAMP while bacterioplankton appear more likely to use deformylated FAMP, 4-amino-5-aminomethyl-2-methylpyrimidine. Measurements of FAMP in seawater and biomass revealed that it occurs at picomolar concentrations in the surface ocean, heterotrophic bacterial cultures produce FAMP in the dark—indicating non-photodegradation of B1 by cells, and B1-requiring (auxotrophic) picoeukaryotic phytoplankton produce intracellular FAMP. Our results require an expansion of thinking about vitamin degradation in the sea, but also the marine B1 cycle where it is now crucial to consider a new B1-related compound pool (FAMP), as well as generation (dark degradation—likely via oxidation), turnover (plankton uptake), and exchange of the compound within the networks of plankton. IMPORTANCEResults of this collaborative study newly show that a vitamin B1 degradation product, N-formyl-4-amino-5-aminomethyl-2-methylpyrimidine (FAMP), can be used by diverse marine microbes (bacteria and phytoplankton) to meet their vitamin B1 demands instead of B1 and that FAMP occurs in the surface ocean. FAMP has not yet been accounted for in the ocean and its use likely enables cells to avoid B1 growth deficiency. Additionally, we show FAMP is formed in and out of cells without solar irradiance—a commonly considered route of vitamin degradation in the sea and nature. Altogether, the results expand thinking about oceanic vitamin degradation, but also the marine B1 cycle where it is now crucial to consider a new B1-related compound pool (FAMP), as well as its generation (dark degradation—likely via oxidation), turnover (plankton uptake), and exchange within networks of plankton.