Central carbon metabolism and electron transport in Chlamydomonas reinhardtii, metabolic constraints for carbon partitioning between oil and starch
TL;DR: As microalgae are now considered a potential renewable feedstock, current work on the subject is examined and the possibility of rerouting metabolism toward lipid production is explored, to compare starch and lipids as carbon reserves.
Abstract: The metabolism of microalgae is so flexible that it is not an easy task to give a comprehensive description of the interplay between the various metabolic pathways. There are, however, constraints that govern central carbon metabolism in Chlamydomonas reinhardtii that are revealed by the compartmentalization and regulation of the pathways and their relation to key cellular processes such as cell motility, division, carbon uptake and partitioning, external and internal rhythms, and nutrient stress. Both photosynthetic and mitochondrial electron transfer provide energy for metabolic processes and how energy transfer impacts metabolism and vice versa is a means of exploring the regulation and function of these pathways. A key example is the specific chloroplast localization of glycolysis/gluconeogenesis and how it impacts the redox poise and ATP budget of the plastid in the dark. To compare starch and lipids as carbon reserves, their value can be calculated in terms of NAD(P)H and ATP. As microalgae are now considered a potential renewable feedstock, we examine current work on the subject and also explore the possibility of rerouting metabolism toward lipid production.
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TL;DR: The review considers the potential of microalgae to produce a range of products and indicates future directions for developing suitable criteria for choosing novel isolates through bioprospecting large gene pool of microalga obtained from various habitats and climatic conditions.
Abstract: Microalgal species are potential resource of both biofuels and high-value metabolites, and their production is growth dependent. Growth parameters can be screened for the selection of novel microalgal species that produce molecules of interest. In this context our review confirms that, autotrophic and heterotrophic organisms have demonstrated a dual potential, namely the ability to produce lipids as well as value-added products (particularly carotenoids) under influence of various physico-chemical stresses on microalgae. Some species of microalgae can synthesize, besides some pigments, very-long-chain polyunsaturated fatty acids (VL-PUFA,>20C) such as docosahexaenoic acid and eicosapentaenoic acid, those have significant applications in food and health. Producing value-added by-products in addition to biofuels, fatty acid methyl esters (FAME), and lipids has the potential to improve microalgae-based biorefineries by employing either the autotrophic or the heterotrophic mode, which could be an offshoot of biotechnology. The review considers the potential of microalgae to produce a range of products and indicates future directions for developing suitable criteria for choosing novel isolates through bioprospecting large gene pool of microalga obtained from various habitats and climatic conditions.
335 citations
Cites background from "Central carbon metabolism and elect..."
...Various stress factors induce changes in the metabolic activities of a cell such as activation of starch and accumulation of TAGs leading to accumulation of lipid bodies in algae (Johnson and Alric, 2013)....
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TL;DR: A critical account of micro-algae as an important step in wastewater treatment for enhancing the reduction of N, P and the chemical oxygen demand in wastewater, whilst utilising a fraction of the energy demand of conventional biological treatment systems.
318 citations
Cites background from "Central carbon metabolism and elect..."
...In photoautotrophic mode, the inorganic carbon fixed in the Calvin cycle can enter the glycolytic pathway (also known as the EmbdenMeyerhof pathway) as G3P, in which it becomesmetabolised into pyruvate (Perez-Garcia et al., 2011b; Johnson and Alric, 2013) (Fig....
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TL;DR: The heterotrophic metabolic potential of microalgae and their uses in pigment production are comprehensively described and strategies to enhance pigment production underheterotrophic conditions are critically discussed and the challenges faced in heterotrophe pigment production with possible alternative solutions are presented.
269 citations
Cites background or methods from "Central carbon metabolism and elect..."
...It has been reported that Chlamydomonas chloroplasts can export 3-phosphoglycerate, dihydroxyacetone phosphate, hexose phosphates and glycolate in the presence of light (Johnson and Alric, 2013)....
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...The conversion can be a single step reaction catalyzed by acetyl CoA synthase or a two-step method involving acetate kinase and phosphate acetyltransferase (Johnson and Alric, 2013)....
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TL;DR: In this article, the authors combined a highly synchronous photobioreactor culture system with frequent temporal sampling to characterize genome-wide diurnal gene expression in Chlamydomonas reinhardtii.
Abstract: The green alga Chlamydomonas reinhardtii is a useful model organism for investigating diverse biological processes, such as photosynthesis and chloroplast biogenesis, flagella and basal body structure/function, cell growth and division, and many others. We combined a highly synchronous photobioreactor culture system with frequent temporal sampling to characterize genome-wide diurnal gene expression in Chlamydomonas. Over 80% of the measured transcriptome was expressed with strong periodicity, forming 18 major clusters. Genes associated with complex structures and processes, including cell cycle control, flagella and basal bodies, ribosome biogenesis, and energy metabolism, all had distinct signatures of coexpression with strong predictive value for assigning and temporally ordering function. Importantly, the frequent sampling regime allowed us to discern meaningful fine-scale phase differences between and within subgroups of genes and enabled the identification of a transiently expressed cluster of light stress genes. Coexpression was further used both as a data-mining tool to classify and/or validate genes from other data sets related to the cell cycle and to flagella and basal bodies and to assign isoforms of duplicated enzymes to their cognate pathways of central carbon metabolism. Our diurnal coexpression data capture functional relationships established by dozens of prior studies and are a valuable new resource for investigating a variety of biological processes in Chlamydomonas and other eukaryotes.
219 citations
Cites background from "Central carbon metabolism and elect..."
...Experimental localization of biochemical activities has been described for some enzymes (reviewed in Johnson and Alric, 2013), but the pathways within which many enzyme isoforms act in Chlamydomonas remain unknown....
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TL;DR: In this article, the authors developed tools in the model alga Chlamydomonas reinhardtii to determine the localizations of 135 candidate CO2-concentrating mechanism proteins and physical interactors of 38 proteins.
214 citations
Cites background from "Central carbon metabolism and elect..."
...PFK is a key regulator of glycolysis and is important for maintaining cellular ATP levels (Johnson and Alric, 2013)....
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References
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TL;DR: A brief summary of the current knowledge on oleaginous algae and their fatty acid and TAG biosynthesis, algal model systems and genomic approaches to a better understanding of TAG production, and a historical perspective and path forward for microalgae-based biofuel research and commercialization are provided.
Abstract: Microalgae represent an exceptionally diverse but highly specialized group of micro-organisms adapted to various ecological habitats. Many microalgae have the ability to produce substantial amounts (e.g. 20-50% dry cell weight) of triacylglycerols (TAG) as a storage lipid under photo-oxidative stress or other adverse environmental conditions. Fatty acids, the building blocks for TAGs and all other cellular lipids, are synthesized in the chloroplast using a single set of enzymes, of which acetyl CoA carboxylase (ACCase) is key in regulating fatty acid synthesis rates. However, the expression of genes involved in fatty acid synthesis is poorly understood in microalgae. Synthesis and sequestration of TAG into cytosolic lipid bodies appear to be a protective mechanism by which algal cells cope with stress conditions, but little is known about regulation of TAG formation at the molecular and cellular level. While the concept of using microalgae as an alternative and renewable source of lipid-rich biomass feedstock for biofuels has been explored over the past few decades, a scalable, commercially viable system has yet to emerge. Today, the production of algal oil is primarily confined to high-value specialty oils with nutritional value, rather than commodity oils for biofuel. This review provides a brief summary of the current knowledge on oleaginous algae and their fatty acid and TAG biosynthesis, algal model systems and genomic approaches to a better understanding of TAG production, and a historical perspective and path forward for microalgae-based biofuel research and commercialization.
3,479 citations
"Central carbon metabolism and elect..." refers background in this paper
...ond, high-light-induced oxidative stress may channel a higher percentage of resources into lipid droplets from oxidized membranes (105)....
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University of California, Los Angeles1, United States Department of Energy2, University of Paris3, Duke University4, University of Massachusetts Medical School5, University of California, Berkeley6, Centre national de la recherche scientifique7, University of California, San Francisco8, Sun Yat-sen University9, University of Tennessee Health Science Center10, University of Minnesota11, Iowa State University12, Genetic Information Research Institute13, Salk Institute for Biological Studies14, Stanford University15, University of Liège16, University of Nebraska–Lincoln17, University of Cambridge18, Washington University in St. Louis19, University of Córdoba (Spain)20, Kyoto University21, Carnegie Institution for Science22, National Autonomous University of Mexico23, University of Münster24, École Normale Supérieure25, University of Melbourne26, University of Paris-Sud27, University of Mainz28, Scripps Research Institute29, Ohio State University30, University of Chicago31, University of Jena32, University of Arizona33, Louisiana State University34, University of New Brunswick35, University College London36, University of Potsdam37, Delaware Biotechnology Institute38, Boyce Thompson Institute for Plant Research39, Macquarie University40, Oklahoma State University Center for Health Sciences41, İzmir University of Economics42, Academy of Sciences of the Czech Republic43, Charles University in Prague44, St. Edward's University45, University of Puget Sound46, Hokkaido University47, Tsinghua University48, Washington State University49, Appalachian State University50, Marquette University51
TL;DR: Analyses of the Chlamydomonas genome advance the understanding of the ancestral eukaryotic cell, reveal previously unknown genes associated with photosynthetic and flagellar functions, and establish links between ciliopathy and the composition and function of flagella.
Abstract: Chlamydomonas reinhardtii is a unicellular green alga whose lineage diverged from land plants over 1 billion years ago. It is a model system for studying chloroplast-based photosynthesis, as well as the structure, assembly, and function of eukaryotic flagella (cilia), which were inherited from the common ancestor of plants and animals, but lost in land plants. We sequenced the approximately 120-megabase nuclear genome of Chlamydomonas and performed comparative phylogenomic analyses, identifying genes encoding uncharacterized proteins that are likely associated with the function and biogenesis of chloroplasts or eukaryotic flagella. Analyses of the Chlamydomonas genome advance our understanding of the ancestral eukaryotic cell, reveal previously unknown genes associated with photosynthetic and flagellar functions, and establish links between ciliopathy and the composition and function of flagella.
2,554 citations
"Central carbon metabolism and elect..." refers background in this paper
...fully sequenced (1) and largely annotated, it is accessible for large-...
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TL;DR: It is shown that a substantial photosynthetic advantage is conferred by correct matching of the circadian clock period with that of the external light-dark cycle, which explains why plants gain advantage from circadian control.
Abstract: Circadian clocks are believed to confer an advantage to plants, but the nature of that advantage has been unknown. We show that a substantial photosynthetic advantage is conferred by correct matching of the circadian clock period with that of the external light-dark cycle. In wild type and in long- and short-circadian period mutants of Arabidopsis thaliana, plants with a clock period matched to the environment contain more chlorophyll, fix more carbon, grow faster, and survive better than plants with circadian periods differing from their environment. This explains why plants gain advantage from circadian control.
1,276 citations
"Central carbon metabolism and elect..." refers background in this paper
...It may be due to an optimization of reserve mobilization (115) or due to multiple effects affecting growth rates like the circadian control on photosynthetic yield resulting in reduced CO2 fixation (116)....
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TL;DR: This paper used mass spectrometry to identify proteins in purified flagella from the green alga Chlamydomonas reinhardtii and found that flagellum is rich in motor and signal transduction components, and contains numerous proteins with homologues associated with diseases such as cystic kidney disease, male sterility, and hydrocephalus in humans and model vertebrates.
Abstract: Cilia and flagella are widespread cell organelles that have been highly conserved throughout evolution and play important roles in motility, sensory perception, and the life cycles of eukaryotes ranging from protists to humans. Despite the ubiquity and importance of these organelles, their composition is not well known. Here we use mass spectrometry to identify proteins in purified flagella from the green alga Chlamydomonas reinhardtii. 360 proteins were identified with high confidence, and 292 more with moderate confidence. 97 out of 101 previously known flagellar proteins were found, indicating that this is a very complete dataset. The flagellar proteome is rich in motor and signal transduction components, and contains numerous proteins with homologues associated with diseases such as cystic kidney disease, male sterility, and hydrocephalus in humans and model vertebrates. The flagellum also contains many proteins that are conserved in humans but have not been previously characterized in any organism. The results indicate that flagella are far more complex than previously estimated.
999 citations
"Central carbon metabolism and elect..." refers background or methods in this paper
...Fructose-1,6-bisphosphate aldolase (ALD) is also reported as mainly chloroplastic because it is absent from the cytosol (35, 44), but it has been also found attached to the flagella (6, 45)....
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...Glyceraldehyde phosphate dehydrogenase, phosphoglycerate kinase, and malate dehydrogenase (MDH) are bound to the flagella, the role of phosphoglycerate kinase being to supply the flagella in ATP, while malate dehydrogenase would regenerate NAD for glyceraldehyde phosphate dehydrogenase turnover (6, 45)....
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...Similarly to that proposed for the flagella in (6, 45), NADP-malate dehydrogenase would regenerate NADP for a partial G3P oxidation by glyceraldehyde phosphate dehydrogenase and dephosphorylation of 1,3BPG, allowing for ATP production in the chloroplast....
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...Following the same reasoning that was used to account for the compartmentalization of the flagellar components (ATP is better off being produced locally) (6, 45), then ATP may have to be produced in the chloroplast by phosphoglycerate kinase to meet the ATP requirements of the preparatory phase of glycolysis....
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..., phosphoglycerate kinase (PGK) and pyruvate kinase, seem attached to the flagella, where ATP production is most needed (6, 45)....
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01 Jun 1996
TL;DR: The regulation of plant glycolytic flux is assessed, with a focus on the fine control of enzymes involved in the metabolism of fructose-6-phosphate and phosphoenolpyruvate.
Abstract: This review discusses the organization and regulation of the glycolytic pathway in plants and compares and contrasts plant and nonplant glycolysis. Plant glycolysis exists both in the cytosol and plastid, and the parallel reactions are catalyzed by distinct nuclear-encoded isozymes. Cytosolic glycolysis is a complex network containing alternative enzymatic reactions. Two alternate cytosolic reactions enhance the pathway's ATP yield through the use of pyrophosphate in place of ATP. The cytosolic glycolytic network may provide an essential metabolic flexibility that facilitates plant development and acclimation to environmental stress. The regulation of plant glycolytic flux is assessed, with a focus on the fine control of enzymes involved in the metabolism of fructose-6-phosphate and phosphoenolpyruvate. Plant and nonplant glycolysis are regulated from the "bottom up" and "top down," respectively. Research on tissue- and developmental-specific isozymes of plant glycolytic enzymes is summarized. Potential pitfalls associated with studies of glycolytic enzymes are considered. Some glycolytic enzymes may be multifunctional proteins involved in processes other than carbohydrate metabolism.
842 citations
"Central carbon metabolism and elect..." refers background in this paper
...Plants seem to have duplicated the entire glycolytic and oxidative pentose-phosphate pathways in the chloroplast and cytosol (38, 39), and plant chloroplasts also possess an efficient export system for hexoses (glucose and maltose transporters [40]) and triose phosphate (phosphate translocator [41, 42])....
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