Comparative Genomics of the Baltic Sea Toxic Cyanobacteria Nodularia spumigena UHCC 0039 and Its Response to Varying Salinity

Abstract

Salinity is an important abiotic factor controlling the distribution and abundance of Nodularia spumigena, the dominating diazotrophic and toxic phototroph, in the brackish water cyanobacterial blooms of the Baltic Sea. To expand the available genomic information for brackish water cyanobacteria, we sequenced the isolate Nodularia spumigena UHCC 0039 using an Illumina-SMRT hybrid sequencing approach, revealing a chromosome of 5,294,286 base pairs (bp) and a single plasmid of 92,326 bp. Comparative genomics in Nostocales showed pronounced genetic similarity among Nodularia spumigena strains evidencing their short evolutionary history. The studied Baltic Sea strains share similar sets of CRISPR-Cas cassettes and a higher number of insertion sequence (IS) elements compared to Nodularia spumigena CENA596 isolated from a shrimp production pond in Brazil. Nodularia spumigena UHCC 0039 proliferated similarly at three tested salinities, whereas the lack of salt inhibited its growth and triggered transcriptome remodeling, including the up-regulation of five sigma factors and the down-regulation of two other sigma factors, one of which is specific for strain UHCC 0039. Down-regulated genes additionally included a large genetic region for the synthesis of two yet unidentified natural products. Our results indicate a remarkable plasticity of the Nodularia salinity acclimation, and thus salinity strongly impacts the intensity and distribution of cyanobacterial blooms in the Baltic Sea.

Genomic and Metabolomic Analyses of Natural Products in Nodularia spumigena Isolated from a Shrimp Culture Pond

“…The subsystem annotation of the genomes revealed a similar pattern of functional annotation. This result point to a noticeable genetic similarity as found in a previous comparative study of the N. spumigena strains [49]. The majority of the orthologs from the four genomes remain unidentified, whereas those that were annotated were involved in key metabolic pathways necessary for the survival of the organisms but also adaptive advantages and the secondary metabolism.…”

“…The approach used in our present work requires genome sequences of the organisms, only four of which are available for Nodularia. Although the two available MAGs of Nodularia were included, we were unable to conduct a robust analysis of the evolutionary relationship of this genus and therefore our analysis resembled a previous analysis constructed with 31 conserved proteins [49]. So far, no evident geographical difference among American, European, and Asian Nodularia can be pointed out.…”

“…Although cyanobacteria naturally compete with algae in aquaculture tanks, cyanobacteria often dominate eutrophic tanks due to their higher ability to thrive with low dissolved oxygen, high temperature, and turbidity [56]. Moreover, the water salinities commonly used in shrimp ponds are optimal for N. spumigena growth [49,[57][58][59]. Therefore, cyanobacteria may form blooms in these environments and negatively interfere with shrimp production [60].…”

“…During the summer, N. spumigena blooms overcome phosphorous limitation by degrading phosphonate and are favored in the Baltic Sea due to stable, stratified, and warm brackish water [46,48]. Strain UHCC 0039 (also known as AV1) was isolated from a water sample collected in 1987 from the open Gulf of Finland [48,49].…”

“…The strain N. spumigena CCY9414, with a possibly complete published genome, was isolated from a sample of brackish surface water collected in 1996 from the Baltic Sea near Bornholm [46,61] (accession number GCF_000340565.2). Strain N. spumigena UHCC 0039 (or N. spumigena AV1), with a complete genome, was isolated from a water sample collected in 1987 from the open Gulf of Finland [12,48,49] (accession number GCF_003054475.1). The draft genome of the Japanese strain Nodularia sp.…”