Insights into the Physiology and Ecology of the Brackish-Water-Adapted Cyanobacterium Nodularia spumigena CCY9414 Based on a Genome-Transcriptome Analysis

Abstract

Nodularia spumigena is a filamentous diazotrophic cyanobacterium that dominates the annual late summer cyanobacterial blooms in the Baltic Sea. But N. spumigena also is common in brackish water bodies worldwide, suggesting special adaptation allowing it to thrive at moderate salinities. A draft genome analysis of N. spumigena sp. CCY9414 yielded a single scaffold of 5,462,271 nucleotides in length on which genes for 5,294 proteins were annotated. A subsequent strand-specific transcriptome analysis identified more than 6,000 putative transcriptional start sites (TSS). Orphan TSSs located in intergenic regions led us to predict 764 non-coding RNAs, among them 70 copies of a possible retrotransposon and several potential RNA regulators, some of which are also present in other N2-fixing cyanobacteria. Approximately 4% of the total coding capacity is devoted to the production of secondary metabolites, among them the potent hepatotoxin nodularin, the linear spumigin and the cyclic nodulapeptin. The transcriptional complexity associated with genes involved in nitrogen fixation and heterocyst differentiation is considerably smaller compared to other Nostocales. In contrast, sophisticated systems exist for the uptake and assimilation of iron and phosphorus compounds, for the synthesis of compatible solutes, and for the formation of gas vesicles, required for the active control of buoyancy. Hence, the annotation and interpretation of this sequence provides a vast array of clues into the genomic underpinnings of the physiology of this cyanobacterium and indicates in particular a competitive edge of N. spumigena in nutrient-limited brackish water ecosystems.

Transcriptomic and Proteomic Profiling of Anabaena sp. Strain 90 under Inorganic Phosphorus Stress

“…Hypothetical proteins and proteins with unknown function are widely abundant among cyanobacterial genome annotations, representing the relatively incomplete knowledge of the metabolism and molecular structure of cyanobacteria (13,27). In this study, we found 5 (5hNP), 11 (6dNP), and 19 (4dLP) proteins with unknown function with more than 4-fold transcriptional changes compared with the controls (log 2 FC Ͼ2 or ϽϪ2; P Յ 0.05).…”

“…Intergenic regions may give rise to sRNAs, another type of important regulatory factors with an important role in physiological adaption and as a driver of interstrain divergence in bacteria, including cyanobacteria (33,34,(49)(50)(51). Studies of the filamentous and nitrogen-fixing cyanobacterium Nodularia spumigena CCY9414 genome and its acclimation to stress conditions point further sRNAs crucial role in cell functioning, especially in gene expression regulation (13,52). Due to their importance as regulatory factors, we searched intergenic regions differentially expressed under phosphorus deprivation conditions.…”

“…Highaffinity P i transporter systems PstABCS, similar to those in Escherichia coli, were found in numerous cyanobacteria and enable phosphorus uptake over a wide range of concentrations (12). In addition, several cyanobacterial genomes encode phosphorus acquisition and assimilation mechanisms for alternative phosphorus sources, such as organic phosphate, phosphonate, and phosphites (13)(14)(15)(16)(17)(18), but the complete functioning of these mechanisms is still unclear (19).…”

Salt acclimation of Nodularia spumigena CCY9414—a cyanobacterium adapted to brackish water

“…PCC 7119; Porchia & Salerno 1996) and has been discussed as the main reason restricting these cyanobacteria to freshwater and brackish water conditions (Hagemann 2011). The genome of Nodularia CCY9414 also harbors genes for the synthesis of trehalose by the TreYZ pathway (Voß et al 2013). However, we never detected trehalose in cell extracts of salt-treated Nodularia CCY9414.…”

“…For this purpose, we used the Baltic Sea isolate N. spumigena CCY9414 (hereafter Nodularia CCY9414), taking advantage of its known genome sequence (GenBank accession no. AAVW 00000000; Voß et al 2013). Genome searches revealed that Nodularia CCY9414 is potentially able to synthesize sucrose as well as trehalose as compatible solutes.…”