Metabolic and Transcriptomic Phenotyping of Inorganic Carbon Acclimation in the Cyanobacterium <i>Synechococcus elongatus</i> PCC 7942

Schwarz, Doreen; Nodop, Anke; Hüge, Jan; Purfürst, Stephanie; Forchhammer, Karl; Michel, Klaus-Peter; Bauwe, Hermann; Kopka, Joachim; Hagemann, Martin

doi:10.1104/pp.110.170225

Cited by 86 publications

(136 citation statements)

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“…CcmR can regulate transcription of several C i uptake genes. In Synechocystis PCC 6803, CcmR appeared to be a repressor of sbtA and the high-affinity CO 2 uptake operon but not of bicA (29,47). In contrast, in Synechococcus PCC 7002, CcmR appeared to be a repressor of bicA and sbtA and possibly the high-affinity CO 2 uptake operon (48,50).…”

Section: Evaluation Of Hypothesesmentioning

confidence: 74%

“…Previously, the CCM genes of the model cyanobacteria Synechocystis PCC 6803, Synechococcus PCC 7002, and Synechococcus 7942 were studied in detail (15,19,(27)(28)(29)(30)(44)(45)(46)(47)(48). Comparison of the CCM genes of our Microcystis strains with these model cyanobacteria reveals several similarities and differences (Tables 2 and 3).…”

Section: Evaluation Of Hypothesesmentioning

confidence: 99%

“…4). Synechocystis PCC 6803 and Synechococcus PCC 7942 use another transcriptional regulator, CmpR, for the cmpABCD operon (27,47), which is absent from Microcystis. CcmR2 is the most likely transcriptional regulator for the bicA and sbtA genes in Microcystis, given the location of ccmR2 upstream of the bicA-sbtA operon (17).…”

Section: Evaluation Of Hypothesesmentioning

confidence: 99%

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Strains of the Harmful Cyanobacterium Microcystis aeruginosa Differ in Gene Expression and Activity of Inorganic Carbon Uptake Systems at Elevated CO ₂ Levels

Sandrini

Jakupovic

Matthijs

et al. 2015

Appl Environ Microbiol

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Cyanobacteria are generally assumed to be effective competitors at low CO 2 levels because of their efficient CO 2 -concentrating mechanism (CCM), and yet how bloom-forming cyanobacteria respond to rising CO 2 concentrations is less clear. Here, we investigate changes in CCM gene expression at ambient CO 2 (400 ppm) and elevated CO 2 (1,100 ppm) in six strains of the harmful cyanobacterium Microcystis. All strains downregulated cmpA encoding the high-affinity bicarbonate uptake system BCT1, whereas both the low-and high-affinity CO 2 uptake genes were expressed constitutively. Four strains downregulated the bicarbonate uptake genes bicA and/or sbtA, whereas two strains showed constitutive expression of the bicA-sbtA operon. In one of the latter strains, a transposon insert in bicA caused low bicA and sbtA transcript levels, which made this strain solely dependent on BCT1 for bicarbonate uptake. Activity measurements of the inorganic carbon (C i ) uptake systems confirmed the CCM gene expression results. Interestingly, genes encoding the RuBisCO enzyme, structural carboxysome components, and carbonic anhydrases were not regulated. Hence, Microcystis mainly regulates the initial uptake of inorganic carbon, which might be an effective strategy for a species experiencing strongly fluctuating C i concentrations. Our results show that CCM gene regulation of Microcystis varies among strains. The observed genetic and phenotypic variation in CCM responses may offer an important template for natural selection, leading to major changes in the genetic composition of harmful cyanobacterial blooms at elevated CO 2 .C O 2 concentrations in the atmosphere may double during this century (1). In marine ecosystems, enhanced dissolution of atmospheric CO 2 causes ocean acidification (2, 3). In freshwaters, however, CO 2 concentrations may vary widely. In many lakes, the dissolved CO 2 concentration exceeds the concentration expected from equilibrium with the atmosphere due to the input of large amounts of organic carbon from terrestrial systems (4, 5). Conversely, the photosynthetic activity of dense phytoplankton blooms can deplete the CO 2 concentration far below atmospheric levels, which increases pH and makes bicarbonate the most abundant inorganic carbon species (6-8). Cyanobacteria are often considered to be very successful competitors at low CO 2 levels (9, 10), and global warming is predicted to favor an expansion of cyanobacterial blooms in eutrophic waters (11-13). However, the response of bloom-forming cyanobacteria to elevated CO 2 levels is not yet well understood.Cyanobacteria typically use a CO 2 -concentrating mechanism (CCM) with up to five different uptake systems for inorganic carbon (C i ): three for bicarbonate and two for CO 2 uptake (14). The two sodium-dependent bicarbonate uptake systems, BicA and SbtA, are present in some but not all freshwater cyanobacteria (15-17). BicA combines a low affinity for bicarbonate with a high flux rate, whereas SbtA usually has a high affinity for bicarbonate but a low flux r...

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Section: Evaluation Of Hypothesesmentioning

confidence: 74%

Section: Evaluation Of Hypothesesmentioning

confidence: 99%

See 1 more Smart Citation

Strains of the Harmful Cyanobacterium Microcystis aeruginosa Differ in Gene Expression and Activity of Inorganic Carbon Uptake Systems at Elevated CO ₂ Levels

Sandrini

Jakupovic

Matthijs

et al. 2015

Appl Environ Microbiol

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“…For example, the two S. elongatus CP12 proteins, CP12-C and CP12-N/C, in addition to differences in potential interaction with GAPDH (Fig. 5) show differences in overall expression under constant light and in response to a shift from high to low atmospheric CO 2 (Schwarz et al, 2011;Vijayan et al, 2011). In Synechocystis sp.…”

Section: Discussionmentioning

confidence: 99%

Comparative Analysis of 126 Cyanobacterial Genomes Reveals Evidence of Functional Diversity Among Homologs of the Redox-Regulated CP12 Protein

2012

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CP12 is found almost universally among photosynthetic organisms, where it plays a key role in regulation of the Calvin cycle by forming a ternary complex with glyceraldehyde 3-phosphate dehydrogenase (GAPDH) and phosphoribulokinase. Newly available genomic sequence data for the phylum Cyanobacteria reveals a heretofore unobserved diversity in cyanobacterial CP12 proteins. Cyanobacterial CP12 proteins can be classified into eight different types based on primary structure features. Among these are CP12-CBS (for cystathionine-b-synthase) domain fusions. CBS domains are regulatory modules for a wide range of cellular activities; many of these bind adenine nucleotides through a conserved motif that is also present in the CBS domains fused to CP12. In addition, a survey of expression data sets shows that the CP12 paralogs are differentially regulated. Furthermore, modeling of the cyanobacterial CP12 protein variants based on the recently available three-dimensional structure of the canonical cyanobacterial CP12 in complex with GAPDH suggests that some of the newly identified cyanobacterial CP12 types are unlikely to bind to GAPDH. Collectively these data show that, as is becoming increasingly apparent for plant CP12 proteins, the role of CP12 in cyanobacteria is likely more complex than previously appreciated, possibly involving other signals in addition to light. Moreover, our findings substantiate the proposal that this small protein may have multiple roles in photosynthetic organisms.

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“…MC1 and MC2 also contain a number of benzoate compounds that have been detected previously in cyanobacteria, including benzoic acid and 4-hydroxybenzoate (4HB) (Fig. S4 and Dataset S2) (38). Recent work has shown that plastoquinone biosynthesis in cyanobacteria uses 4HB as an intermediate (39,40).…”

Section: Correlations In Metabolite Abundance Can Help Classify Unknownmentioning

confidence: 99%

The circadian oscillator in Synechococcus elongatus controls metabolite partitioning during diurnal growth

Diamond

Jun

Rubin

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

124

158

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Synechococcus elongatus PCC 7942 is a genetically tractable model cyanobacterium that has been engineered to produce industrially relevant biomolecules and is the best-studied model for a prokaryotic circadian clock. However, the organism is commonly grown in continuous light in the laboratory, and data on metabolic processes under diurnal conditions are lacking. Moreover, the influence of the circadian clock on diurnal metabolism has been investigated only briefly. Here, we demonstrate that the circadian oscillator influences rhythms of metabolism during diurnal growth, even though lightdark cycles can drive metabolic rhythms independently. Moreover, the phenotype associated with loss of the core oscillator protein, KaiC, is distinct from that caused by absence of the circadian output transcriptional regulator, RpaA (regulator of phycobilisome-associated A). Although RpaA activity is important for carbon degradation at night, KaiC is dispensable for those processes. Untargeted metabolomics analysis and glycogen kinetics suggest that functional KaiC is important for metabolite partitioning in the morning. Additionally, output from the oscillator functions to inhibit RpaA activity in the morning, and kaiC-null strains expressing a mutant KaiC phosphomimetic, KaiC-pST, in which the oscillator is locked in the most active output state, phenocopies a ΔrpaA strain. Inhibition of RpaA by the oscillator in the morning suppresses metabolic processes that normally are active at night, and kaiC-null strains show indications of oxidative pentose phosphate pathway activation as well as increased abundance of primary metabolites. Inhibitory clock output may serve to allow secondary metabolite biosynthesis in the morning, and some metabolites resulting from these processes may feed back to reinforce clock timing.C yanobacteria comprise a promising engineering platform for the production of fuels and industrial chemicals. These organisms already have been engineered to produce ethanol, isobutyraldehyde, alkanes, and hydrogen (1-4). However, the efficient industrial-scale application of these photosynthetic organisms will require their growth and maintenance in the outdoors where they will be subjected to light-dark (LD) cycles (5). Phototrophic cyanobacteria present a completely different engineering challenge relative to heterotrophic bacteria such as Escherichia coli: their cellular activities respond strongly to the presence and absence of light because their metabolism is centered on photosynthesis (6, 7). Diverse cyanobacteria also possess a true circadian clock that synchronizes with external LD cycles and has been demonstrated to drive both gene expression and metabolic rhythms (8-10). It is important to understand how signals from the external environment and the internal circadian clock are integrated to modulate metabolic processes in environmentally relevant LD cycles to optimize the engineering of these organisms. In this work we attempt to separate the influences of environment and circadian control using the cyan...

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Metabolic and Transcriptomic Phenotyping of Inorganic Carbon Acclimation in the Cyanobacterium Synechococcus elongatus PCC 7942

Cited by 86 publications

References 51 publications

Strains of the Harmful Cyanobacterium Microcystis aeruginosa Differ in Gene Expression and Activity of Inorganic Carbon Uptake Systems at Elevated CO ₂ Levels

Strains of the Harmful Cyanobacterium Microcystis aeruginosa Differ in Gene Expression and Activity of Inorganic Carbon Uptake Systems at Elevated CO ₂ Levels

Comparative Analysis of 126 Cyanobacterial Genomes Reveals Evidence of Functional Diversity Among Homologs of the Redox-Regulated CP12 Protein

The circadian oscillator in Synechococcus elongatus controls metabolite partitioning during diurnal growth

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Metabolic and Transcriptomic Phenotyping of Inorganic Carbon Acclimation in the Cyanobacterium Synechococcus elongatus PCC 7942

Cited by 86 publications

References 51 publications

Strains of the Harmful Cyanobacterium Microcystis aeruginosa Differ in Gene Expression and Activity of Inorganic Carbon Uptake Systems at Elevated CO 2 Levels

Strains of the Harmful Cyanobacterium Microcystis aeruginosa Differ in Gene Expression and Activity of Inorganic Carbon Uptake Systems at Elevated CO 2 Levels

Comparative Analysis of 126 Cyanobacterial Genomes Reveals Evidence of Functional Diversity Among Homologs of the Redox-Regulated CP12 Protein

The circadian oscillator in Synechococcus elongatus controls metabolite partitioning during diurnal growth

Contact Info

Product

Resources

About

Strains of the Harmful Cyanobacterium Microcystis aeruginosa Differ in Gene Expression and Activity of Inorganic Carbon Uptake Systems at Elevated CO ₂ Levels

Strains of the Harmful Cyanobacterium Microcystis aeruginosa Differ in Gene Expression and Activity of Inorganic Carbon Uptake Systems at Elevated CO ₂ Levels