A Metabolomic Approach to Study Major Metabolite Changes during Acclimation to Limiting CO2 in <i>Chlamydomonas reinhardtii</i>

Renberg, Linda; Johansson, Ann-Sofi; Shutova, Tatiana; Stenlund, Hans; Aksmann, Anna; Raven, John A.; Gardeström, Per; Moritz, Thomas; Samuelsson, Göran

doi:10.1104/pp.110.157651

Cited by 82 publications

(63 citation statements)

References 56 publications

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“…In this particular situation we hypothesize that the increase in these enzymes compensates the loss of activity related to the low temperatures. In contrast, aspartate and glutamate, recently reported to be decreased during under low CO 2 (106), are two-and sixfold increased after 24 h following an opposite trend. Furthermore the low CO 2 induced proteins LCIB, shown to function downstream of CAH3 in the CCM in the vicinity of the pyrenoid (107), and LCI5, a stromal protein with unknown function (108), reported to be constantly expressed during non CO 2 enriched cultures situations are reduced during cold exposure.…”

Section: Discussionmentioning

confidence: 85%

Systemic Cold Stress Adaptation of Chlamydomonas reinhardtii

Valledor

Furuhashi

Hanak

et al. 2013

Molecular & Cellular Proteomics

126

128

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Chlamydomonas reinhardtii is one of the most important model organisms nowadays phylogenetically situated between higher plants and animals (Merchant et al. 2007). Stress adaptation of this unicellular model algae is in the focus because of its relevance to biomass and biofuel production. Here, we have studied cold stress adaptation of C. reinhardtii hitherto not described for this algae whereas intensively studied in higher plants. Toward this goal, high throughput mass spectrometry was employed to integrate proteome, metabolome, physiological and cell-morphological changes during a time-course from 0 to 120 h. These data were complemented with RT-qPCR for target genes involved in central metabolism, signaling, and lipid biosynthesis. Using this approach dynamics in central metabolism were linked to cold-stress dependent sugar and autophagy pathways as well as novel genes in C. reinhardtii such as CKIN1, CKIN2 and a hitherto functionally not annotated protein named CKIN3. Cold stress affected extensively the physiology and the organization of the cell. Gluconeogenesis and starch biosynthesis pathways are activated leading to a pronounced starch and sugar accumulation. Quantitative lipid profiles indicate a sharp decrease in the lipophilic fraction and an increase in polyunsaturated fatty acids suggesting this as a mechanism of maintaining membrane fluidity. The proteome is completely remodeled during cold stress: specific candidates of the ribosome and the spliceosome indicate altered biosynthesis and degradation of proteins important for adaptation to low temperatures. Specific proteasome degradation may be mediated by the observed cold-specific changes in the ubiquitinylation system. Sparse partial least squares regression analysis was applied for protein correlation network analysis using proteins as predictors and Fv/Fm, FW, total lipids, and starch as responses. We applied also Granger causality analysis and revealed correlations between proteins and metabolites otherwise not detectable. Twenty percent of the proteins responsive to cold are uncharacterized proteins. This presents a considerable resource for new discoveries in cold stress biology in alga and plants. Molecular &

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Section: Discussionmentioning

confidence: 85%

Systemic Cold Stress Adaptation of Chlamydomonas reinhardtii

Valledor

Furuhashi

Hanak

et al. 2013

Molecular & Cellular Proteomics

126

128

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“…Thus, Ferredoxin-NADP + reductase, which has been identified in proteins spots 9 and 10 from S. platensis proteome (Table 1), is a enzyme involved in the active transportation of HCO 3 -from the external environment for assimilation of CO 2 inside the carboxysomes through the conversion of these HCO 3 -ions by CA (Guedeney et al 1996, Giordano et al 2005). In C. reinhardtii, a variety of CA genes, especially mitochondrial CA, have been implicated for expression only under low-CO 2 condition (Yamano et al 2008, Renberg et al 2010, Baba et al 2011, Fang et al 2012. However, further studies are required to understand whether ferredoxin-NADP + reductase implicated in this study is mitochondrial or membrane bound.…”

Section: Spirulina Platensis: Control Vs Exposed Samplementioning

confidence: 99%

“…Recently, C. reinhardtii proteome, transcriptome and metabolome have been studied under varying CO 2 concentration. Cumulatively, these studies suggest the involvement of novel transport proteins involved in C i transport and also reveal the effect of induction of CCM on whole genome (Yamano et al 2008, Renberg et al 2010, Baba et al 2011, Fang et al 2012). However, effect of CO 2 on other green alga and cynaobacteria has not been investigated so far.…”

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confidence: 99%

Influence of CO₂concentration on carbon concentrating mechanisms in cyanobacteria and green algae: a proteomic approach

Ramanan¹,

Vinayagamoorthy²,

Sivanesan³

et al. 2012

ALGAE

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Carbon concentrating mechanisms play a vital role in photosynthesis in microalgae and cyanobacteria especially in the proper functioning of Rubisco and assimilation of carbon via the Calvin cycle. This study evaluates the role of carbon dioxide on carbon concentrating mechanism (CCM) in a cynaobacteria, Spirulina platensis and a microalga, Chlorella sp. 786. The study organisms were grown in both atmospheric (control sample, 0.035%) and high (exposed sample, 10%) CO 2 concentrations. Second dimension (2D) electrophoresis revealed a huge difference in the protein profiles of both organisms suggesting the induction of CCM related proteins in the sample maintained at atmospheric CO 2 concentration and the repression of CCM related proteins in the sample maintained at 10% CO 2 . Liquid chromatography-mass spectroscopy analysis revealed the presence of two important C i transporter proteins in the control sample of S. platensis, namely ferredoxin-NADP + reductase and ATP binding cassette (ABC) transport system protein. These proteins were only expressed in the control sample and were downregulated or not expressed at all in the exposed sample. Consequently, this study conclusively proves that CCMs are only inducted at low CO 2 concentrations and are not functional at high CO 2 concentration.Key Words: carbon concentrating mechanism (CCM); Chlorella sp.; cyanobacteria; proteomics; Rubisco; Spirulina platensis INTRODUCTIONNatural photosynthesis in green plants achieves carbon dioxide (CO 2 ) fixation on a global scale. The incorporation of CO 2 into the biosphere by the photosynthetic action of plants and microorganisms has been estimated to amount to about 10 11 tons of CO 2 per year Somanchi 1999, Prentice 2001). However, the efficiency of solar energy conversion in plant production under optimal growth conditions is only 5-6%. The global average efficiency has been estimated as 0.15% (Price et al. 2008). Photosynthesis is much more efficient in single celled organisms such as microalgae and cyanobacteria than in terrestrial C 3 and C 4 plants ( Kaplan and Reinhold 1999). This high efficiency is primarily due to two factors: the action of carbonic anhydrase (CA), both extracellular and intracellular, and the CO 2 concentrating mechanisms (CCM) ( Van et al. 2001, Spalding et al. 2002, Vance and Spalding 2005. CO 2 concentration plays a vital role in the induction or repression of CCM in microalgae and cyanobacteria. It has been proven that CCM is induced in low CO 2 concentrations, however, there is little informa- 296exposed sample was maintained at a CO 2 concentration of 10% (10,000 ppm). Both the cultures were grown for a period of 15-20 days in the reactor (Ramanan et al. 2010).The algal cells were centrifuged at 5,000 ×g for 5 min and to 0.5 g of algal pellet, 10 mL of algal culture medium with 2% Triton X-100 was added. The algal pellet was resuspended and pelleted. Supernatant which had greenish-yellow tint was poured off. The pellet was once again rinsed with culture medium and centrifuged again. The super...

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“…Regulation here means the changes to the functioning of the pre-existing proteome (changes in post-translational modification and in ligand concentration) over times of seconds to minutes of a change in conditions: there is not enough time for changes to the proteome, related to changes in transcription and translation. Acclimation is defined as changes in the use of the existing genome by changes in transcription and translation, and hence in the proteome and metabolome (Raven 2010(Raven , 2011Renberg et al 2010;Wienkoop et al 2010), in response to changes in the environment; it occurs over time intervals of an hour and longer, and occurs in parallel with, and may modulate, regulation. Adaptation is taken to mean evolutionary changes to the genome in response to changed environmental conditions, with the possibility of more extreme changes to the proteome and metabolome than is the case for acclimation.…”

Section: General Considerationsmentioning

confidence: 99%

“…Since then very significant progress has been made in relating CCMs to the range of kinetics of Rubisco (ribulose bisphosphate carboxylase-oxygenase) in cyanobacteria, algae and aquatic plants, to the species of inorganic carbon entering the cells, the roles of carbonic anhydrase and the possibility of C 4 -like photosynthetic metabolism in cyanobacteria, algae and aquatic plants (Giordano et al 2005;Raven 2010Raven , 2011Renberg et al 2010). The molecular genetic basis of CCMs in cyanobacteria is now relatively well understood, with some understanding of the genetic basis of eukaryotic CCMs (Raven 2010(Raven , 2011.…”

Section: Introductionmentioning

confidence: 99%

Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change

et al. 2011

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Abstract.Carbon dioxide concentrating mechanisms (also known as inorganic carbon concentrating mechanisms; both abbreviated as CCMs) presumably evolved under conditions of low CO 2 availability. However, the timing of their origin is unclear since there are no sound estimates from molecular clocks, and even if there were, there are no proxies for the functioning of CCMs. Accordingly, we cannot use previous episodes of high CO 2 (e.g. the Palaeocene-Eocene Thermal Maximum) to indicate how organisms with CCMs responded. Present and predicted environmental change in terms of increased CO 2 and temperature are leading to increased CO 2 and HCO 3 -and decreased CO 3 2-and pH in surface seawater, as well as decreasing the depth of the upper mixed layer and increasing the degree of isolation of this layer with respect to nutrient flux from deeper waters. The outcome of these forcing factors is to increase the availability of inorganic carbon, photosynthetic active radiation (PAR) and ultraviolet B radiation (UVB) to aquatic photolithotrophs and to decrease the supply of the nutrients (combined) nitrogen and phosphorus and of any non-aeolian iron. The influence of these variations on CCM expression has been examined to varying degrees as acclimation by extant organisms. Increased PAR increases CCM expression in terms of CO 2 affinity, while increased UVB has a range of effects in the organisms examined; little relevant information is available on increased temperature. Decreased combined nitrogen supply generally increases CO 2 affinity, decreased iron availability increases CO 2 affinity, and decreased phosphorus supply has varying effects on the organisms examined. There are few data sets showing interactions among the observed changes, and even less information on genetic (adaptation) 2 changes in response to the forcing factors. In freshwaters, changes in phytoplankton species composition may alter with environmental change with consequences for frequency of species with or without CCMs. The information available permits less predictive power as to the effect of the forcing factors on CCM expression than for their overall effects on growth. CCMs are currently not part of models as to how global environmental change has altered, and is likely to further alter, algal and aquatic plant primary productivity.Keywords CO 2 concentrating mechanism -combined nitrogen -inorganic carboniron -mixing depth -photosynthetically active radiation -phosphorus -temperature -UVA-UVB Abbreviations CCM CO 2 concentrating mechanism DOC Dissolved organic carbon PAR Photosynthetically active radiation (400-700 nm)Rubisco Ribulose bisphosphate carboxylase-oxygenase UVA Ultraviolet A radiation (320-400 nm) UVB Ultraviolet B radiation (280-320 nm)

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A Metabolomic Approach to Study Major Metabolite Changes during Acclimation to Limiting CO2 in Chlamydomonas reinhardtii

Cited by 82 publications

References 56 publications

Systemic Cold Stress Adaptation of Chlamydomonas reinhardtii

Systemic Cold Stress Adaptation of Chlamydomonas reinhardtii

Influence of CO₂concentration on carbon concentrating mechanisms in cyanobacteria and green algae: a proteomic approach

Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change

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A Metabolomic Approach to Study Major Metabolite Changes during Acclimation to Limiting CO2 in Chlamydomonas reinhardtii

Cited by 82 publications

References 56 publications

Systemic Cold Stress Adaptation of Chlamydomonas reinhardtii

Systemic Cold Stress Adaptation of Chlamydomonas reinhardtii

Influence of CO2concentration on carbon concentrating mechanisms in cyanobacteria and green algae: a proteomic approach

Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change

Contact Info

Product

Resources

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Influence of CO₂concentration on carbon concentrating mechanisms in cyanobacteria and green algae: a proteomic approach