Chlamydomonas Cell Biology

A special issue of Cells (ISSN 2073-4409). This special issue belongs to the section "Plant, Algae and Fungi Cell Biology".

Deadline for manuscript submissions: closed (15 October 2019) | Viewed by 65404

Special Issue Editor


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Guest Editor
Institute of Plant Biochemistry and Photosynthesis (IBVF-CSIC), 41092 Sevilla, Spain
Interests: TOR signaling; autophagy; redox control of autophagy; Chlamydomonas; microalgae

Special Issue Information

Dear Colleagues,

The unicellular green alga, Chlamydomonas reinhardtii, is a powerful model system for studying central processes in photosynthetic eukaryotes, including chloroplast biogenesis, photosynthesis, motility, light perception and cell cycle control. The availability of an annotated nuclear genome and a growing array of tools and techniques for molecular genetic studies have boosted research on fundamental questions in the cell and molecular biology of this model organism. In this Special Issue of Cells, we solicit your contributions in the form of reviews, original research articles or shorter “perspective” articles on all aspects related with Chlamydomonas cell biology, such as plastid biogenesis, cell signalling, biofuel production, carbon metabolism, nutrient assimilation, flagella biology, organelle structure or vacuole function.

Dr. Jose L. Crespo
Guest Editor

Manuscript Submission Information

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Keywords

  • Chlamydomonas
  • model organism
  • microalga
  • chloroplast
  • cell signaling
  • autophagy
  • lipid metabolism
  • flagella
  • carbon
  • photosynthesis assimilation

Published Papers (12 papers)

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Research

Jump to: Review

24 pages, 5233 KiB  
Article
Evidence Supporting an Antimicrobial Origin of Targeting Peptides to Endosymbiotic Organelles
by Clotilde Garrido, Oliver D. Caspari, Yves Choquet, Francis-André Wollman and Ingrid Lafontaine
Cells 2020, 9(8), 1795; https://doi.org/10.3390/cells9081795 - 28 Jul 2020
Cited by 17 | Viewed by 3983
Abstract
Mitochondria and chloroplasts emerged from primary endosymbiosis. Most proteins of the endosymbiont were subsequently expressed in the nucleo-cytosol of the host and organelle-targeted via the acquisition of N-terminal presequences, whose evolutionary origin remains enigmatic. Using a quantitative assessment of their physico-chemical properties, [...] Read more.
Mitochondria and chloroplasts emerged from primary endosymbiosis. Most proteins of the endosymbiont were subsequently expressed in the nucleo-cytosol of the host and organelle-targeted via the acquisition of N-terminal presequences, whose evolutionary origin remains enigmatic. Using a quantitative assessment of their physico-chemical properties, we show that organelle targeting peptides, which are distinct from signal peptides targeting other subcellular compartments, group with a subset of antimicrobial peptides. We demonstrate that extant antimicrobial peptides target a fluorescent reporter to either the mitochondria or the chloroplast in the green alga Chlamydomonas reinhardtii and, conversely, that extant targeting peptides still display antimicrobial activity. Thus, we provide strong computational and functional evidence for an evolutionary link between organelle-targeting and antimicrobial peptides. Our results support the view that resistance of bacterial progenitors of organelles to the attack of host antimicrobial peptides has been instrumental in eukaryogenesis and in the emergence of photosynthetic eukaryotes. Full article
(This article belongs to the Special Issue Chlamydomonas Cell Biology)
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21 pages, 2744 KiB  
Article
Metabolic, Physiological, and Transcriptomics Analysis of Batch Cultures of the Green Microalga Chlamydomonas Grown on Different Acetate Concentrations
by Kenny A. Bogaert, Emilie Perez, Judith Rumin, Axel Giltay, Michele Carone, Nadine Coosemans, Michele Radoux, Gauthier Eppe, Raphael D. Levine, Francoise Remacle and Claire Remacle
Cells 2019, 8(11), 1367; https://doi.org/10.3390/cells8111367 - 31 Oct 2019
Cited by 22 | Viewed by 3807
Abstract
Acetate can be efficiently metabolized by the green microalga Chlamydomonas reinhardtii. The regular concentration is 17 mM, although higher concentrations are reported to increase starch and fatty acid content. To understand the responses to higher acetate concentrations, Chlamydomonas cells were cultivated in [...] Read more.
Acetate can be efficiently metabolized by the green microalga Chlamydomonas reinhardtii. The regular concentration is 17 mM, although higher concentrations are reported to increase starch and fatty acid content. To understand the responses to higher acetate concentrations, Chlamydomonas cells were cultivated in batch mode in the light at 17, 31, 44, and 57 mM acetate. Metabolic analyses show that cells grown at 57 mM acetate possess increased contents of all components analyzed (starch, chlorophylls, fatty acids, and proteins), with a three-fold increased volumetric biomass yield compared to cells cultivated at 17 mM acetate at the entry of stationary phase. Physiological analyses highlight the importance of photosynthesis for the low-acetate and exponential-phase samples. The stationary phase is reached when acetate is depleted, except for the cells grown at 57 mM acetate, which still divide until ammonium exhaustion. Surprisal analysis of the transcriptomics data supports the biological significance of our experiments. This allows the establishment of a model for acetate assimilation, its transcriptional regulation and the identification of candidates for genetic engineering of this metabolic pathway. Altogether, our analyses suggest that growing at high-acetate concentrations could increase biomass productivities in low-light and CO2-limiting air-bubbled medium for biotechnology. Full article
(This article belongs to the Special Issue Chlamydomonas Cell Biology)
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18 pages, 2791 KiB  
Article
Cell Cycle Arrest by Supraoptimal Temperature in the Alga Chlamydomonas reinhardtii
by Vilém Zachleder, Ivan Ivanov, Milada Vítová and Kateřina Bišová
Cells 2019, 8(10), 1237; https://doi.org/10.3390/cells8101237 - 11 Oct 2019
Cited by 22 | Viewed by 3983
Abstract
Temperature is one of the key factors affecting growth and division of algal cells. High temperature inhibits the cell cycle in Chlamydomonas reinhardtii. At 39 °C, nuclear and cellular divisions in synchronized cultures were blocked completely, while DNA replication was partly affected. [...] Read more.
Temperature is one of the key factors affecting growth and division of algal cells. High temperature inhibits the cell cycle in Chlamydomonas reinhardtii. At 39 °C, nuclear and cellular divisions in synchronized cultures were blocked completely, while DNA replication was partly affected. In contrast, growth (cell volume, dry matter, total protein, and RNA) remained unaffected, and starch accumulated at very high levels. The cell cycle arrest could be removed by transfer to 30 °C, but a full recovery occurred only in cultures cultivated up to 14 h at 39 °C. Thereafter, individual cell cycle processes began to be affected in sequence; daughter cell release, cell division, and DNA replication. Cell cycle arrest was accompanied by high mitotic cyclin-dependent kinase activity that decreased after completion of nuclear and cellular division following transfer to 30 °C. Cell cycle arrest was, therefore, not caused by a lack of cyclin-dependent kinase activity but rather a blockage in downstream processes. Full article
(This article belongs to the Special Issue Chlamydomonas Cell Biology)
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22 pages, 2900 KiB  
Article
Inhibition of TOR in Chlamydomonas reinhardtii Leads to Rapid Cysteine Oxidation Reflecting Sustained Physiological Changes
by Megan M. Ford, Amanda L. Smythers, Evan W. McConnell, Sarah C. Lowery, Derrick R. J. Kolling and Leslie M. Hicks
Cells 2019, 8(10), 1171; https://doi.org/10.3390/cells8101171 - 28 Sep 2019
Cited by 21 | Viewed by 4785
Abstract
The target of rapamycin (TOR) kinase is a master metabolic regulator with roles in nutritional sensing, protein translation, and autophagy. In Chlamydomonas reinhardtii, a unicellular green alga, TOR has been linked to the regulation of increased triacylglycerol (TAG) accumulation, suggesting that TOR [...] Read more.
The target of rapamycin (TOR) kinase is a master metabolic regulator with roles in nutritional sensing, protein translation, and autophagy. In Chlamydomonas reinhardtii, a unicellular green alga, TOR has been linked to the regulation of increased triacylglycerol (TAG) accumulation, suggesting that TOR or a downstream target(s) is responsible for the elusive “lipid switch” in control of increasing TAG accumulation under nutrient limitation. However, while TOR has been well characterized in mammalian systems, it is still poorly understood in photosynthetic systems, and little work has been done to show the role of oxidative signaling in TOR regulation. In this study, the TOR inhibitor AZD8055 was used to relate reversible thiol oxidation to the physiological changes seen under TOR inhibition, including increased TAG content. Using oxidized cysteine resin-assisted capture enrichment coupled with label-free quantitative proteomics, 401 proteins were determined to have significant changes in oxidation following TOR inhibition. These oxidative changes mirrored characterized physiological modifications, supporting the role of reversible thiol oxidation in TOR regulation of TAG production, protein translation, carbohydrate catabolism, and photosynthesis through the use of reversible thiol oxidation. The delineation of redox-controlled proteins under TOR inhibition provides a framework for further characterization of the TOR pathway in photosynthetic eukaryotes. Full article
(This article belongs to the Special Issue Chlamydomonas Cell Biology)
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13 pages, 1609 KiB  
Communication
Dynamic Interactions between Autophagosomes and Lipid Droplets in Chlamydomonas reinhardtii
by Quynh-Giao Tran, Hyang Ran Yoon, Kichul Cho, Seon-Jin Lee, José L. Crespo, Rishiram Ramanan and Hee-Sik Kim
Cells 2019, 8(9), 992; https://doi.org/10.3390/cells8090992 - 28 Aug 2019
Cited by 22 | Viewed by 5665
Abstract
Autophagy is a highly conserved catabolic process in eukaryotic cells by which waste cellular components are recycled to maintain growth in both favorable and stress conditions. Autophagy has been linked to lipid metabolism in microalgae; however, the mechanism underlying this interaction remains unclear. [...] Read more.
Autophagy is a highly conserved catabolic process in eukaryotic cells by which waste cellular components are recycled to maintain growth in both favorable and stress conditions. Autophagy has been linked to lipid metabolism in microalgae; however, the mechanism underlying this interaction remains unclear. In this study, transgenic Chlamydomonas reinhardtii cells that stably express the red fluorescent protein (mCherry) tagged-ATG8 as an autophagy marker were established. By using this tool, we were able to follow the autophagy process in live microalgal cells under various conditions. Live-cell and transmission electron microscopy (TEM) imaging revealed physical contacts between lipid droplets and autophagic structures during the early stage of nitrogen starvation, while fusion of these two organelles was observed in prolonged nutritional deficiency, suggesting that an autophagy-related pathway might be involved in lipid droplet turnover in this alga. Our results thus shed light on the interplay between autophagy and lipid metabolism in C. reinhardtii, and this autophagy marker would be a valuable asset for further investigations on autophagic processes in microalgae. Full article
(This article belongs to the Special Issue Chlamydomonas Cell Biology)
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12 pages, 2806 KiB  
Article
Truncated Hemoglobins 1 and 2 Are Implicated in the Modulation of Phosphorus Deficiency-Induced Nitric Oxide Levels in Chlamydomonas
by Valentina Filina, Alexandra Grinko and Elena Ermilova
Cells 2019, 8(9), 947; https://doi.org/10.3390/cells8090947 - 21 Aug 2019
Cited by 12 | Viewed by 2744
Abstract
Truncated hemoglobins (trHbs) form a widely distributed family of proteins found in archaea, bacteria, and eukaryotes. Accumulating evidence suggests that trHbs may be implicated in functions other than oxygen delivery, but these roles are largely unknown. Characterization of the conditions that affect trHb [...] Read more.
Truncated hemoglobins (trHbs) form a widely distributed family of proteins found in archaea, bacteria, and eukaryotes. Accumulating evidence suggests that trHbs may be implicated in functions other than oxygen delivery, but these roles are largely unknown. Characterization of the conditions that affect trHb expression and investigation of their regulatory mechanisms will provide a framework for elucidating the functions of these globins. Here, the transcription of Chlamydomonas trHb genes (THB112) under conditions of phosphorus (P) deprivation was analyzed. Three THB genes, THB1, THB2, and THB12 were expressed at the highest level. For the first time, we demonstrate the synthesis of nitric oxide (NO) under P-limiting conditions and the production of NO by cells via a nitrate reductase-independent pathway. To clarify the functions of THB1 and THB2, we generated and analyzed strains in which these THBs were strongly under-expressed by using an artificial microRNA approach. Similar to THB1 knockdown, the depletion of THB2 led to a decrease in cell size and chlorophyll levels. We provide evidence that the knockdown of THB1 or THB2 enhanced NO production under P deprivation. Overall, these results demonstrate that THB1 and THB2 are likely to contribute, at least in part, to acclimation responses in P-deprived Chlamydomonas. Full article
(This article belongs to the Special Issue Chlamydomonas Cell Biology)
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15 pages, 2842 KiB  
Article
Response of the Green Alga Chlamydomonas reinhardtii to the DNA Damaging Agent Zeocin
by Mária Čížková, Monika Slavková, Milada Vítová, Vilém Zachleder and Kateřina Bišová
Cells 2019, 8(7), 735; https://doi.org/10.3390/cells8070735 - 17 Jul 2019
Cited by 13 | Viewed by 4031
Abstract
DNA damage is a ubiquitous threat endangering DNA integrity in all living organisms. Responses to DNA damage include, among others, induction of DNA repair and blocking of cell cycle progression in order to prevent transmission of damaged DNA to daughter cells. Here, we [...] Read more.
DNA damage is a ubiquitous threat endangering DNA integrity in all living organisms. Responses to DNA damage include, among others, induction of DNA repair and blocking of cell cycle progression in order to prevent transmission of damaged DNA to daughter cells. Here, we tested the effect of the antibiotic zeocin, inducing double stranded DNA breaks, on the cell cycle of synchronized cultures of the green alga Chlamydomonas reinhardtii. After zeocin application, DNA replication partially occurred but nuclear and cellular divisions were completely blocked. Application of zeocin combined with caffeine, known to alleviate DNA checkpoints, decreased cell viability significantly. This was probably caused by a partial overcoming of the cell cycle progression block in such cells, leading to aberrant cell divisions. The cell cycle block was accompanied by high steady state levels of mitotic cyclin-dependent kinase activity. The data indicate that DNA damage response in C. reinhardtii is connected to the cell cycle block, accompanied by increased and stabilized mitotic cyclin-dependent kinase activity. Full article
(This article belongs to the Special Issue Chlamydomonas Cell Biology)
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Review

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26 pages, 1781 KiB  
Review
Algae-Bacteria Consortia as a Strategy to Enhance H2 Production
by Neda Fakhimi, David Gonzalez-Ballester, Emilio Fernández, Aurora Galván and Alexandra Dubini
Cells 2020, 9(6), 1353; https://doi.org/10.3390/cells9061353 - 29 May 2020
Cited by 40 | Viewed by 4443
Abstract
Biological hydrogen production by microalgae is a potential sustainable, renewable and clean source of energy. However, many barriers limiting photohydrogen production in these microorganisms remain unsolved. In order to explore this potential and make biohydrogen industrially affordable, the unicellular microalga Chlamydomonas reinhardtii is [...] Read more.
Biological hydrogen production by microalgae is a potential sustainable, renewable and clean source of energy. However, many barriers limiting photohydrogen production in these microorganisms remain unsolved. In order to explore this potential and make biohydrogen industrially affordable, the unicellular microalga Chlamydomonas reinhardtii is used as a model system to solve barriers and identify new approaches that can improve hydrogen production. Recently, Chlamydomonas–bacteria consortia have opened a new window to improve biohydrogen production. In this study, we review the different consortia that have been successfully employed and analyze the factors that could be behind the improved H2 production. Full article
(This article belongs to the Special Issue Chlamydomonas Cell Biology)
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16 pages, 1287 KiB  
Review
Salinity Stress Responses and Adaptation Mechanisms in Eukaryotic Green Microalgae
by Prateek Shetty, Margaret Mukami Gitau and Gergely Maróti
Cells 2019, 8(12), 1657; https://doi.org/10.3390/cells8121657 - 17 Dec 2019
Cited by 164 | Viewed by 10891
Abstract
High salinity is a challenging environmental stress for organisms to overcome. Unicellular photosynthetic microalgae are especially vulnerable as they have to grapple not only with ionic imbalance and osmotic stress but also with the generated reactive oxygen species (ROS) interfering with photosynthesis. This [...] Read more.
High salinity is a challenging environmental stress for organisms to overcome. Unicellular photosynthetic microalgae are especially vulnerable as they have to grapple not only with ionic imbalance and osmotic stress but also with the generated reactive oxygen species (ROS) interfering with photosynthesis. This review attempts to compare and contrast mechanisms that algae, particularly the eukaryotic Chlamydomonas microalgae, exhibit in order to immediately respond to harsh conditions caused by high salinity. The review also collates adaptation mechanisms of freshwater algae strains under persistent high salt conditions. Understanding both short-term and long-term algal responses to high salinity is integral to further fundamental research in algal biology and biotechnology. Full article
(This article belongs to the Special Issue Chlamydomonas Cell Biology)
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19 pages, 2308 KiB  
Review
Good News for Nuclear Transgene Expression in Chlamydomonas
by Michael Schroda
Cells 2019, 8(12), 1534; https://doi.org/10.3390/cells8121534 - 28 Nov 2019
Cited by 54 | Viewed by 5815
Abstract
Chlamydomonas reinhardtii is a well-established model system for basic research questions ranging from photosynthesis and organelle biogenesis, to the biology of cilia and basal bodies, to channelrhodopsins and photoreceptors. More recently, Chlamydomonas has also been recognized as a suitable host for the production [...] Read more.
Chlamydomonas reinhardtii is a well-established model system for basic research questions ranging from photosynthesis and organelle biogenesis, to the biology of cilia and basal bodies, to channelrhodopsins and photoreceptors. More recently, Chlamydomonas has also been recognized as a suitable host for the production of high-value chemicals and high-value recombinant proteins. However, basic and applied research have suffered from the inefficient expression of nuclear transgenes. The combined efforts of the Chlamydomonas community over the past decades have provided insights into the mechanisms underlying this phenomenon and have resulted in mutant strains defective in some silencing mechanisms. Moreover, many insights have been gained into the parameters that affect nuclear transgene expression, like promoters, introns, codon usage, or terminators. Here I critically review these insights and try to integrate them into design suggestions for the construction of nuclear transgenes that are to be expressed at high levels. Full article
(This article belongs to the Special Issue Chlamydomonas Cell Biology)
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16 pages, 1284 KiB  
Review
When Unity Is Strength: The Strategies Used by Chlamydomonas to Survive Environmental Stresses
by Félix de Carpentier, Stéphane D. Lemaire and Antoine Danon
Cells 2019, 8(11), 1307; https://doi.org/10.3390/cells8111307 - 23 Oct 2019
Cited by 43 | Viewed by 7299
Abstract
The unicellular green alga Chlamydomonas reinhardtii is a valuable model system to study a wide spectrum of scientific fields, including responses to environmental conditions. Most studies are performed under optimal growth conditions or under mild stress. However, when environmental conditions become harsher, the [...] Read more.
The unicellular green alga Chlamydomonas reinhardtii is a valuable model system to study a wide spectrum of scientific fields, including responses to environmental conditions. Most studies are performed under optimal growth conditions or under mild stress. However, when environmental conditions become harsher, the behavior of this unicellular alga is less well known. In this review we will show that despite being a unicellular organism, Chlamydomonas can survive very severe environmental conditions. To do so, and depending on the intensity of the stress, the strategies used by Chlamydomonas can range from acclimation to the formation of multicellular structures, or involve programmed cell death. Full article
(This article belongs to the Special Issue Chlamydomonas Cell Biology)
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15 pages, 976 KiB  
Review
Subcellular Energetics and Carbon Storage in Chlamydomonas
by Adrien Burlacot, Gilles Peltier and Yonghua Li-Beisson
Cells 2019, 8(10), 1154; https://doi.org/10.3390/cells8101154 - 26 Sep 2019
Cited by 19 | Viewed by 6120
Abstract
Microalgae have emerged as a promising platform for production of carbon- and energy- rich molecules, notably starch and oil. Establishing an economically viable algal biotechnology sector requires a holistic understanding of algal photosynthesis, physiology, cell cycle and metabolism. Starch/oil productivity is a combined [...] Read more.
Microalgae have emerged as a promising platform for production of carbon- and energy- rich molecules, notably starch and oil. Establishing an economically viable algal biotechnology sector requires a holistic understanding of algal photosynthesis, physiology, cell cycle and metabolism. Starch/oil productivity is a combined effect of their cellular content and cell division activities. Cell growth, starch and fatty acid synthesis all require carbon building blocks and a source of energy in the form of ATP and NADPH, but with a different requirement in ATP/NADPH ratio. Thus, several cellular mechanisms have been developed by microalgae to balance ATP and NADPH supply which are essentially produced by photosynthesis. Major energy management mechanisms include ATP production by the chloroplast-based cyclic electron flow and NADPH removal by water-water cycles. Furthermore, energetic coupling between chloroplast and other cellular compartments, mitochondria and peroxisome, is increasingly recognized as an important process involved in the chloroplast redox poise. Emerging literature suggests that alterations of energy management pathways affect not only cell fitness and survival, but also influence biomass content and composition. These emerging discoveries are important steps towards diverting algal photosynthetic energy to useful products for biotechnological applications. Full article
(This article belongs to the Special Issue Chlamydomonas Cell Biology)
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