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

Voß, Björn; Bolhuis, Henk; Fewer, David P.; Kopf, Matthias; Möke, Fred; Haas, Fabian B.; El-Shehawy, Rehab; Hayes, Paul K.; Bergman, Birgitta; Sivonen, Kaarina; Dittmann, Elke; Scanlan, David J.; Hagemann, Martin; Stal, Lucas J.; Hess, Wolfgang R.

doi:10.1371/journal.pone.0060224

Cited by 79 publications

(79 citation statements)

References 162 publications

(193 reference statements)

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…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).…”

Section: Resultsmentioning

confidence: 57%

“…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.…”

Section: Resultsmentioning

confidence: 99%

“…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).…”

mentioning

confidence: 99%

See 2 more Smart Citations

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

Teikari

Österholm

Kopf

et al. 2015

Appl Environ Microbiol

Self Cite

View full text Add to dashboard Cite

cInorganic phosphorus (P i ) is one of the main growth-limiting factors of diazotrophic cyanobacteria. Due to human activity, the availability of P i has increased in water bodies, resulting in eutrophication and the formation of massive cyanobacterial blooms. In this study, we examined the molecular responses of the cyanobacterium Anabaena sp. strain 90 to phosphorus deprivation, aiming at the identification of candidate genes to monitor the P i status in cyanobacteria. Furthermore, this study increased the basic understanding of how phosphorus affects diazotrophic and bloom-forming cyanobacteria as a major growth-limiting factor. Based on RNA sequencing data, we identified 246 differentially expressed genes after phosphorus starvation and 823 differentially expressed genes after prolonged P i limitation, most of them related to central metabolism and cellular growth. The transcripts of the genes related to phosphorus transport and assimilation (pho regulon) were most upregulated during phosphorus depletion. One of the most increased transcripts encodes a giant protein of 1,869 amino acid residues, which contains, among others, a phytase-like domain. Our findings predict its crucial role in phosphorus starvation, but future studies are still needed. Using twodimensional difference in gel electrophoresis (2D-DIGE) and liquid chromatography-tandem mass spectrometry (LC-MS/MS), we found 43 proteins that were differentially expressed after prolonged phosphorus stress. However, correlation analysis unraveled an association only to some extent between the transcriptomic and proteomic abundances. Based on the present results, we suggest that the method used for monitoring the P i status in cyanobacterial bloom should contain wider combinations of pho regulon genes (e.g., PstABCS transport systems) in addition to the commonly used alkaline phosphatase gene alone. N itrogen and phosphorus loading into aquatic ecosystems is a global problem causing enhanced primary production of photoautotrophic organisms (1-3). Among them, cyanobacteria are major beneficiaries of turbid and eutrophic water. They employ numerous ecophysiological strategies such as the capability for using various nutrient sources, gas vacuoles, photoprotective pigments, and UV-absorbing compounds, which enable them to survive and grow under eutrophic conditions and may lead to the formation of harmful and toxic blooms (1, 4). The theory that nutrient loading is a crucial factor causing harmful cyanobacterial blooms is supported by numerous field and laboratory studies showing that toxin production and growth rate both increase under nutrient-replete conditions (2, 5-8).The diazotrophic Anabaena is one of the most common bloomforming cyanobacterial genera in freshwater and brackish-water ecosystems, alongside Microcystis and Nodularia, respectively (4, 9), and some strains are capable of producing the following toxins: microcystins, anatoxin-a, anatoxin-a(S), and saxitoxins (4, 10). The ecology of these cyanobacteria thus deserves more attention. The abil...

show abstract

Section: Resultsmentioning

confidence: 57%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

See 1 more Smart Citation

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

Teikari

Österholm

Kopf

et al. 2015

Appl Environ Microbiol

Self Cite

View full text Add to dashboard Cite

show abstract

“…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.…”

Section: Discussionmentioning

confidence: 99%

“…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.…”

Section: Abstract: Compatible Solute · Glutamate · Potassium · Sucrosementioning

confidence: 99%

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

Möke¹,

Wasmund²,

Bauwe³

et al. 2013

Aquat. Microb. Ecol.

View full text Add to dashboard Cite

The toxic cyanobacterium Nodularia spumigena regularly forms large surface blooms in the central Baltic Sea. The Baltic Sea is characterized by a salinity gradient. We analyzed the salt acclimation of the strain N. spumigena CCY9414, the only Nodularia strain with a known genome sequence. N. spumigena CCY9414 showed a rather low salt tolerance range, displaying a growth optimum at 12.5 g NaCl l −1. Sucrose was identified as the major compatible solute. The expression of the sucrose-phosphate synthase gene was salt-stimulated, which indicates that the salt-induced sucrose accumulation could be regulated at the transcriptional level. Potassium ions and glutamate were also accumulated in Nodularia cells, especially at high salinities when sucrose levels were rather low. Our results indicate that N. spumigena CCY9414 represents a truly brackish-water-adapted cyanobacterial strain. KEY WORDS: Compatible solute · Glutamate · Potassium · SucroseResale or republication not permitted without written consent of the publisher Aquat Microb Ecol 70: 207-214, 2013 west connection to the North Sea and almost freshwater conditions in the Northern and Eastern edges (Samuelsson 1996). The distribution of Nodularia spumigena could depend on the external salinity because blooms occur mostly in the central Baltic Sea characterized by brackish waters around 8 practical salinity units (PSU) (Feistel et al. 2010). To adjust the internal osmotic potential to changing salinities, cyanobacteria are known to accumulate specific classes of compatible solutes (Hagemann 2011). Members of the group Nostocales, such as the model strain Anabaena sp. PCC 7119, usually show optimal growth under fresh water conditions and can acclimate to brackish water salinities by the accumulation of sucrose, which is catalyzed by sucrose-phosphate synthase (SPS) (Porchia & Salerno 1996).Compared to freshwater Anabaena strains, Nodularia spumigena seems to prefer brackish water conditions. To get deeper insight into the basic saltacclimation strategy of this ecologically important cyanobacterial genus, we aimed to investigate the salt response of N. spumigena under defined laboratory conditions. 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. Our results suggest that Nodularia CCY9414 is a brackish-water-adapted cyanobacterium because it grew optimally at salinities around 10 g NaCl l −1 and accumulated sucrose as the main compatible solute under these conditions. MATERIALS AND METHODS Strain and cultivationNodularia spumigena CCY9414 was obtained from the Culture Collection Yerseke (CCY) at the Netherlands Institute of Sea Research (NIOZ). This Baltic Sea strain was isolated from surface waters of ~9 PSU east of the island of Bornholm. It was taken into the strain ...

show abstract

Current Understanding of the Regulatory Roles ofmiRNAs for Enhancing Photosynthesis in Plants Under Environmental Stresses

Hussain

Irfan

et al. 2019

Photosynthesis, Productivity and Environmental Stress

View full text Add to dashboard Cite

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

Cited by 79 publications

References 162 publications

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

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

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

Current Understanding of the Regulatory Roles ofmiRNAs for Enhancing Photosynthesis in Plants Under Environmental Stresses

Contact Info

Product

Resources

About