REVIEW PAPER
Temperature-Induced Photo-Physiological
and Carbon Concentration Mechanism
Responses in Chlamydomonas reinhardtii
More details
Hide details
1
Department of Botany and Microbiology, Acharya Nagarjuna University, Nagarjuna Nagar,
Guntur, Andhra Pradesh, 522510, India
2
Department of Microbiology, Bhaskaracharya College of Applied Sciences, University of Delhi, Delhi, 110075, India
Submission date: 2024-09-19
Final revision date: 2025-02-14
Acceptance date: 2025-03-17
Online publication date: 2025-05-07
Corresponding author
Mallikarjuna Kokkanti
Department of Botany and Microbiology,, Acharya Nagarjuna University, , Nagarjuna Nagar, Andhra Pradesh , India, 522510, Guntur, India
KEYWORDS
TOPICS
ABSTRACT
Heat-trapping of atmospheric high CO2 causes global warming, a censorious parameter that leaves
an antagonistic impression on all photosynthetic organisms’ physiological and productive activities.
To reduce these high CO2 levels, the Carbon Concentration Mechanism (CCM)-based microalgal CO2
mitigation was considered the most efficient non-negative impact method. The photosynthetic regulatory
mechanism of all photoautotrophs is the primary target for high temperatures, resulting in decreased
photosynthesis and productivity rate. Therefore, to counteract high-temperature stress on productivity,
it is necessary to understand the high-temperature acclimation responses of CCM and the photosynthetic
network in the cell at the molecular level. This will provide great insight into how photosynthetic light
and CCM genes network together toward high temperatures for stable photosynthesis. It also increases
the concern over developing thermotolerant strains. This review goes through some of the molecular
responses of the microalgae Chlamydomonas reinharditii, a plant model, to high temperatures.
It discusses how the organism senses heat, initiates protective mechanisms, and alters the expression
of genes related to carbon concentration mechanisms and photosynthesis to acquire thermotolerance.
CONFLICT OF INTEREST
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
REFERENCES (74)
1.
MALLIKARJUNA K., NARENDRA K., RAGALATHA R., RAO B.J. Elucidation and genetic intervention of CO2 concentration mechanism in Chlamydomonas reinhardtii for increased plant primary productivity. Journal of Biosciences, 45, 1, 2020.
https://doi.org/10.1007/s12038... PMid:33051409.
2.
WANG L., YAMANO T., TAKANE S., NIIKAWA Y., TOYOKAWA C., OZAWA S.I., TOKUTSU R., TAKAHASHI Y., MINAGAWA J., KANESAKI Y., YOSHIKAWA H., FUKUZAWA H. Chloroplast-mediated regulation of CO2-concentrating mechanism by Ca2+-binding protein CAS in the green algae Chlamydomonas reinhardtii. Proceedings of the National Academy of Sciences, 113 (44), 12586, 2016.
https://doi.org/10.1073/pnas.1... PMid:27791081 PMCid:PMC5098658.
3.
BAYRO-KAISER V., NELSON N. Temperature sensitive photosynthesis: point mutated CEF-G, PRK, or PsbO act as temperature-controlled switches for essential photosynthetic processes. Frontiers in Plant Science, 11, 562985, 2020.
https://doi.org/10.3389/fpls.2... PMid:33101332 PMCid:PMC7545824.
4.
BOSE H., SATYANARAYANA T. Microbial carbonic anhydrases in biomimetic carbon sequestration for mitigating global warming: prospects and perspectives. Frontiers in Microbiology, 8, 1615, 2017.
https://doi.org/10.3389/fmicb.... PMid:28890712 PMCid:PMC5574912.
6.
ZEREN CETIN I. Used in Urban Area for Landscape Planning and Design Spatial and Temporal Variations in Chromium (Cr) Concentrations in Picea orientalis L. Turkish Journal of Agriculture-Food Science and Technology, 12 (10), 1730, 2024.
https://doi.org/10.24925/turja....
7.
DUMITRU O.A., AUSTERMANN J., POLYAK V.J., FORNÓS J.J., ASMEROM Y., GINÉS J., GINÉS A., ONAC B.P. Constraints on global mean sea level during Pliocene warmth. Nature, 574 (7777), 233, 2019.
https://doi.org/10.1038/s41586... PMid:31471591.
8.
KRISHNAN R., SANJAY J., GNANASEELAN C., MUJUMDAR M., KULKARNI A., CHAKRABORTY S. Assessment of climate change over the Indian region: a report of the ministry of earth sciences (MOES), government of India. Springer Nature, pp. 226, 2020.
https://doi.org/10.1007/978-98....
9.
TRÖSCH R., RIES F., WESTRICH L.D., GAO Y., HERKT C., HOPPSTÄDTER J., HECK-ROTH J., MUSTAS M., SCHEURING D., CHOQUET Y., RÄSCHLE M. Fast and global reorganization of the chloroplast protein biogenesis network during heat acclimation. The Plant Cell, 34 (3), 1075, 2022.
https://doi.org/10.1093/plcell... PMid:34958373 PMCid:PMC8894945.
10.
RIEBSAME W.E. Drought and Natural Resources Management in the United States: impacts and implications of the 1987-89 drought. Routledge, 2019.
https://doi.org/10.4324/978042....
12.
DUSENGE M.E., DUARTE A.G., WAY D.A. Plant carbon metabolism and climate change: elevated CO2 and temperature impacts on photosynthesis, photorespiration and respiration. New Phytologist, 221 (1), 32, 2019.
https://doi.org/10.1111/nph.15... PMid:29983005.
13.
QUADER M.A., AHMED S. Bioenergy with carbon capture and storage (BECCS): Future prospects of carbonnegative technologies. In Clean energy for sustainable development, Academic Press, 91, 2017.
https://doi.org/10.1016/B978-0....
14.
CHOI B.Y., KIM H., SHIM D., JANG S., YAMAOKA Y., SHIN S., YAMANO T., KAJIKAWA M., JIN E., FUKUZAWA H., LEE Y. The Chlamydomonas bZIP transcription factor BLZ8 confers oxidative stress tolerance by inducing the carbon-concentrating mechanism. The Plant Cell, 34 (2), 910, 2022.
https://doi.org/10.1093/plcell... PMid:34893905 PMCid:PMC8824676.
15.
HANSSEN S.V., DAIOGLOU V., STEINMANN Z.J.N., DOELMAN J.C., VAN VUUREN D.P., HUIJBREGTS M.A.J. The climate change mitigation potential of bioenergy with carbon capture and storage. Nature Climate Change, 10 (11), 1023, 2020.
https://doi.org/10.1038/s41558....
17.
BELLIDO-PEDRAZA C.M., TORRES M.J., LLAMAS A. The Microalgae Chlamydomonas for Bioremediation and Bioproduct Production. Cells, 13 (13), 1137, 2024.
https://doi.org/10.3390/cells1... PMid:38994989 PMCid:PMC11240456.
18.
Biofuel: how new microalgae technologies can hasten the end of our reliance on oil. Available online:
https://theconversation.com/bi... (accessed on 24 February 2022).
19.
PATTY C.L., ARIESE F., BUMA W.J., TEN KATE I.L., VAN SPANNING R.J., SNIK F. Circular spectropolarimetric sensing of higher plant and algal chloroplast structural variations. Photosynthesis Research, 140, 129, 2019.
https://doi.org/10.1007/s11120... PMid:30141032 PMCid:PMC6548066.
20.
SALOMÉ P.A., MERCHANT S.S. A series of fortunate events: introducing Chlamydomonas as a reference organism. The Plant Cell, 31 (8), 1682, 2019.
https://doi.org/10.1105/tpc.18... PMid:31189738 PMCid:PMC6713297.
21.
HEMME D., VEYEL D., MÜHLHAUS T., SOMMER F., JÜPPNER J., UNGER A.K., SANDMANN M., FEHRLE I., SCHÖNFELDER S., STEUP M., GEIMER S. Systemswide analysis of acclimation responses to long-term heat stress and recovery in the photosynthetic model organism Chlamydomonas reinhardtii. The Plant Cell, 26 (11), 4270, 2014.
https://doi.org/10.1105/tpc.11... PMid:25415976 PMCid:PMC4277220.
22.
SHI J., HUANG T., CHAI S., GUO Y., WEI J., DOU S., LI L., LIU G. Identification of reference and biomarker proteins in Chlamydomonas reinhardtii cultured under different stress conditions. International Journal of Molecular Sciences, 18 (8), 1822, 2017.
https://doi.org/10.3390/ijms18... PMid:28829403 PMCid:PMC5578208.
23.
BURLACOT A., DAO O., AUROY P., CUINÉ S., LIBEISSON Y., PELTIER G. Alternative photosynthesis pathways drive the algal CO2-concentrating mechanism. Nature, 605 (7909), 366, 2022.
https://doi.org/10.1038/s41586... PMid:35477755.
24.
ADLER L., DÍAZ-RAMOS A., MAO Y., PUKACZ K.R., FEI C., MCCORMICK A.J. New horizons for building pyrenoid-based CO2-concentrating mechanisms in plants to improve yields. Plant Physiology, 190 (3), 1609, 2022.
https://doi.org/10.1093/plphys... PMid:35961043 PMCid:PMC9614477.
25.
PRASAD R., GUPTA S.K., SHABNAM N., OLIVEIRA C.Y.B., NEMA A.K., ANSARI F.A., BUX F. Role of microalgae in global CO2 sequestration: Physiological mechanism, recent development, challenges, and future prospective. Sustainability, 13 (23), 13061, 2021.
https://doi.org/10.3390/su1323....
26.
RAVEN J.A., BEARDALL J., SÁNCHEZ-BARACALDO P. The possible evolution and future of CO2-concentrating mechanisms. Journal of Experimental Botany, 68 (14), 3701, 2017.
https://doi.org/10.1093/jxb/er... PMid:28505361.
27.
YAMANO T., TOYOKAWA C., SHIMAMURA D., MATSUOKA T., FUKUZAWA H. CO2-dependent migration and relocation of LCIB, a pyrenoid-peripheral protein in Chlamydomonas reinhardtii. Plant Physiology, 188 (2), 1081, 2022.
https://doi.org/10.1093/plphys... PMid:34791500 PMCid:PMC8825250.
28.
YAMANO T., SATO E., IGUCHI H., FUKUDA Y., FUKUZAWA H. Characterization of cooperative bicarbonate uptake into chloroplast stroma in the green alga Chlamydomonas reinhardtii. Proceedings of the National Academy of Sciences, 112 (23), 7315, 2015.
https://doi.org/10.1073/pnas.1... PMid:26015566 PMCid:PMC4466737.
29.
SONG Y., CHEN Q., CI D., SHAO X., ZHANG D. Effects of high temperature on photosynthesis and related gene expression in poplar. BMC Plant Biology, 14, 1, 2014.
https://doi.org/10.1186/1471-2... PMid:24774695 PMCid:PMC4036403.
30.
MOORE C.E., MEACHAM-HENSOLD K., LEMONNIER P., SLATTERY R.A., BENJAMIN C., BERNACCHI C.J., LAWSON T., CAVANAGH A.P. The effect of increasing temperature on crop photosynthesis: from enzymes to ecosystems. Journal of Experimental Botany, 72 (8), 2822, 2021.
https://doi.org/10.1093/jxb/er... PMid:33619527 PMCid:PMC8023210.
31.
MA D., LI Y., FU H. Effect of high temperature on the balance between photosynthetic light absorption and energy utilization in Chlorella pyrenoidosa (Chlorophyceae). Journal of Oceanology and Limnology, 38 (1), 186, 2020.
https://doi.org/10.1007/s00343....
32.
YAMAGUCHI D.P., NAKAJI T., HIURA T., HIKOSAKA K. Effects of seasonal change and experimental warming on the temperature dependence of photosynthesis in the canopy leaves of Quercus serrata. Tree Physiology, 36 (10), 1283, 2016.
https://doi.org/10.1093/treeph... PMid:27107017.
33.
LI M., YOUNG J.N. Temperature sensitivity of carbon concentrating mechanisms in the diatom Phaeodactylum tricornutum. Photosynthesis Research, 156 (2), 205, 2023.
https://doi.org/10.1007/s11120... PMid:36881356 PMCid:PMC10154264.
34.
ZHANG N., MATTOON E.M., MCHARGUE W., VENN B., ZIMMER D., PECANI K., JEONG J., ANDERSON C.M., CHEN C., BERRY J.C., XIA M. Systems-wide analysis revealed shared and unique responses to moderate and acute high temperatures in the green alga Chlamydomonas reinhardtii. Communications Biology, 5 (1), 460, 2022.
https://doi.org/10.1038/s42003... PMid:35562408 PMCid:PMC9106746.
35.
SEKIGUCHI M., KAMEDA S., KUROSAWA S., YOSHIDA M., YOSHIMURA K. Thermotaxis in Chlamydomonas is brought about by membrane excitation and controlled by redox conditions. Scientific Reports, 8 (1), 16114, 2018.
https://doi.org/10.1038/s41598... PMid:30382191 PMCid:PMC6208428.
36.
BARATI B., GAN S.Y., LIM P.E., BEARDALL J., PHANG S.M. Green algal molecular responses to temperature stress. Acta Physiologiae Plantarum, 41, 1, 2019.
https://doi.org/10.1007/s11738....
38.
HU S., DING Y., ZHU C. Sensitivity and responses of chloroplasts to heat stress in plants. Frontiers in Plant Science, 11, 375, 2020.
https://doi.org/10.3389/fpls.2... PMid:32300353 PMCid:PMC7142257.
39.
GUIHUR A., REBEAUD M.E., GOLOUBINOFF P. How do plants feel the heat and survive? Trends in Biochemical Sciences, 47 (10), 824, 2022.
https://doi.org/10.1016/j.tibs... PMid:35660289.
40.
SCHMOLLINGER S., SCHULZ-RAFFELT M., STRENKERT D., VEYEL D., VALLON O., SCHRODA M. Dissecting the heat stress response in Chlamydomonas by pharmaceutical and RNAi approaches reveals conserved and novel aspects. Molecular Plant, 6 (6), 1795, 2013.
https://doi.org/10.1093/mp/sst... PMid:23713078.
41.
PIVATO M., BALLOTTARI M. Chlamydomonas reinhardtii cellular compartments and their contribution to intracellular calcium signalling. Journal of Experimental Botany, 72 (15), 5312, 2021.
https://doi.org/10.1093/jxb/er... PMid:34077536 PMCid:PMC8318260.
42.
MCGOLDRICK L.L., SINGH A.K., DEMIRKHANYAN L., LIN T.Y., CASNER R.G., ZAKHARIAN E., SOBOLEVSKY A.I. Structure of the thermo-sensitive TRP channel TRP1 from the alga Chlamydomonas reinhardtii. Nature Communications, 10 (1), 4180, 2019.
https://doi.org/10.1038/s41467... PMid:31519888 PMCid:PMC6744473.
43.
XIE Y., SHEN Q., LI F., NI S., YU J. Temperature response of plants and heat tolerance in Rice: A review. Advances in Agronomy, 179, 135, 2023.
https://doi.org/10.1016/bs.agr....
44.
FIRMANSYAH A.N., ARGOSUBEKTI N. A review of heat stress signaling in plants. In IOP Conference Series: Earth and Environmental Science, IOP Publishing, 484 (1), 012041, 2020.
https://doi.org/10.1088/1755-1....
45.
ZHAO J., LU Z., WANG L., JIN B. Plant responses to heat stress: physiology, transcription, noncoding RNAs, and epigenetics. International Journal of Molecular Sciences, 22 (1), 117, 2020.
https://doi.org/10.3390/ijms22... PMid:33374376 PMCid:PMC7795586.
46.
MITTLER R., FINKA A., GOLOUBINOFF P. How do plants feel the heat? Trends in Biochemical Sciences, 37 (3), 118, 2012.
https://doi.org/10.1016/j.tibs... PMid:22236506.
47.
RÜTGERS M., MURANAKA L.S., MÜHLHAUS T., SOMMER F., THOMS S., SCHURIG J., WILLMUND F., SCHULZ-RAFFELT M., SCHRODA M. Substrates of the chloroplast small heat shock proteins 22E/F point to thermolability as a regulative switch for heat acclimation in Chlamydomonas reinhardtii. Plant Molecular Biology, 95, 579, 2017.
https://doi.org/10.1007/s11103... PMid:29094278 PMCid:PMC5700999.
48.
GROSSMAN A., WOLLMAN F.A. The Chlamydomonas Sourcebook: Organellar and Metabolic Processes. Academic Press, 2, 2023.
49.
VAKULENKO G. The role and regulation of heat shock proteins in the Antarctic alga Chlamydomonas priscuii (Doctoral dissertation, Université d'Ottawa/University of Ottawa), 2022.
50.
SEVGI T., DEMIRKAN E. Effects of calcium concentration, calcium chelators, calcium channel-blockers on Hsp70a expression in Chlamydomonas reinhardtii. Biotech Studies, 31 (1), 10, 2021.
https://doi.org/10.38042/biote....
51.
GJINDALI0 A., JOHNSON G.N. Photosynthetic acclimation to changing environments. Biochemical Society Transactions, 51 (2), 473, 2023.
https://doi.org/10.1042/BST202... PMid:36892145 PMCid:PMC10212544.
53.
LÉGERET B., SCHULZ‐RAFFELT M., NGUYEN H.M., AUROY P., BEISSON F., PELTIER G., BLANC G., LI‐BEISSON Y. Lipidomic and transcriptomic analyses of Chlamydomonas reinhardtii under heat stress unveil a direct route for the conversion of membrane lipids into storage lipids. Plant, Cell & Environment, 39 (4), 834, 2016.
https://doi.org/10.1111/pce.12... PMid:26477535.
54.
IVANOV I.N., ZACHLEDER V., VÍTOVÁ M., BARBOSA M.J., BIŠOVÁ K. Starch production in Chlamydomonas reinhardtii through supraoptimal temperature in a pilotscale photobioreactor. Cells, 10 (5), 1084, 2021.
https://doi.org/10.3390/cells1... PMid:34062892 PMCid:PMC8147326.
55.
MADIREDDI S.K., NAMA S., DEVADASU E., SUBRAMANYAM R. Thylakoid membrane dynamics and state transitions in Chlamydomonas reinhardtii under elevated temperature. Photosynthesis Research, 139, 215, 2019.
https://doi.org/10.1007/s11120... PMid:30030686.
56.
KATO Y., NAGAO R., NOGUCHI T. Redox potential of the terminal quinone electron acceptor QB in photosystem II reveals the mechanism of electron transfer regulation. Proceedings of the National Academy of Sciences, 113 (3), 620, 2016.
https://doi.org/10.1073/pnas.1... PMid:26715751 PMCid:PMC4725517.
57.
TAKAHASHI S., YOSHIOKA-NISHIMURA M., NANBA D., BADGER M.R. Thermal acclimation of the symbiotic alga Symbiodinium spp. alleviates photobleaching under heat stress. Plant Physiol, 161 (1), 477, 2013.
https://doi.org/10.1104/pp.112... PMid:23170037 PMCid:PMC3532276.
58.
PARTHASARATHI T., FIRDOUS S., DAVID E.M., LESHARADEVI K., DJANAGUIRAMAN M. Effects of high temperature on crops. In Advances in plant defense mechanisms. IntechOpen, 2022.
https://doi.org/10.5772/intech....
59.
VIDAL-MEIRELES A., KUNTAM S., SZÉLES E., TÓTH D., NEUPERT J., BOCK R., TÓTH SZ. The lifetime of the oxygen-evolving complex subunit PSBO depends on light intensity and carbon availability in Chlamydomonas. Plant Cell Environ, 46 (2), 422, 2023.
https://doi.org/10.1111/pce.14... PMid:36320098 PMCid:PMC10100022.
60.
CAKMAK I., BROWN P., COLMENERO-FLORES J.M., HUSTED S., KUTMAN B.Y., NIKOLIC M., RENGEL Z., SCHMIDT S.B., ZHAO F.J. Micronutrients. In Marschner's mineral nutrition of plants, Academic Press, 283, 2023.
https://doi.org/10.1016/B978-0....
61.
IVANOV A.G., VELITCHKOVA M.Y., ALLAKHVERDIEV S.I., HUNER N.P.A. Heat stress-induced effects of photosystem I: an overview of structural and functional responses. Photosynth Research, 133, 17, 2017.
https://doi.org/10.1007/s11120... PMid:28391379.
62.
BRICKER T.M., ROOSE J.L., FAGERLUND R.D., FRANKEL L.K., EATON-RYE J.J. The extrinsic proteins of Photosystem II. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1817 (1), 121, 2012.
https://doi.org/10.1016/j.bbab... PMid:21801710.
63.
MATHUR S., AGRAWAL D., JAJOO A. Photosynthesis: response to high temperature stress. Journal of Photochemistry and Photobiology B: Biology, 137, 116, 2014.
https://doi.org/10.1016/j.jpho... PMid:24796250.
65.
WANG Y., STESSMAN D.J., SPALDING M.H. The CO2 concentrating mechanism and photosynthetic carbon assimilation in limiting CO2: how Chlamydomonas works against the gradient. The Plant Journal, 82 (3), 429, 2015.
https://doi.org/10.1111/tpj.12... PMid:25765072.
66.
KATANO T., LEE J., LEE Y.J., KIM M.K., LEE C.G., JIN E.S., KANG S.H., HAN M.S. Effect of temperature on inorganic carbon acquisition of Chlamydomonas reinhardtii. Journal of Freshwater Ecology, 24 (2), 255, 2009.
https://doi.org/10.1080/027050....
67.
RAI A.K., CHEN T., MORONEY J.V. Mitochondrial carbonic anhydrases are needed for optimal photosynthesis at low CO2 levels in Chlamydomonas. Plant Physiology, 187 (3), 1387, 2021.
https://doi.org/10.1093/plphys... PMid:34618049 PMCid:PMC8566214.
68.
MATHUR S., SINGH P., MEHTA P., JAJOO A. Effects of high temperature and low pH on photosystem 2 photochemistry in spinach thylakoid membranes. Biologia Plantarum, 55, 747, 2011.
https://doi.org/10.1007/s10535....
69.
LOVYAGINA E., SEMIN B. Elevation of photosystem II thermal stability at pH 5.7 due to the structural transition in the oxygen-evolving complex. Journal of Plant Biochemistry and Biotechnology, 1, 2021.
https://doi.org/10.1007/s13562... PMCid:PMC10643713.
70.
IGNATOVA L., ZHURIKOVA E., IVANOV B. The presence of the low molecular mass carbonic anhydrase in photosystem II of C3 higher plants. Journal of Plant Physiology, 232, 94, 2019.
https://doi.org/10.1016/j.jplp... PMid:30537617.
71.
SHITOV A.V., TERENTYEV V.V., GOVINDJEE G. Fast enzymatic HCO3-dehydration supports photosynthetic water oxidation in Photosystem II from pea. BioRxiv, 2021.
72.
LEE T.M., TSENG Y.F., CHENG C.L., CHEN Y.C., LIN C.S., SU H.Y., CHOW T.J., CHEN C.Y., CHANG J.S. Characterization of a heat-tolerant Chlorella sp. GD mutant with enhanced photosynthetic CO2 fixation efficiency and its implication as lactic acid fermentation feedstock. Biotechnology for Biofuels, 10, 1, 2017.
https://doi.org/10.1186/s13068... PMid:28919927 PMCid:PMC5596919.
73.
HALPAPE W., WULF D., VERWAAIJEN B., STASCHE A.S., ZENKER S., SIELEMANN J., TSCHIKIN S., VIEHÖVER P., SOMMER M., WEBER A.P., DELKER C. Transcription factors mediating regulation of photosynthesis. BioRxiv, 2023.
https://doi.org/10.1101/2023.0....
74.
HIKOSAKA K., ISHIKAWA K., BORJIGIDAI A., MULLER O., ONODA Y. Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. Journal of Bxperimental Botany, 57 (2), 291, 2006.
https://doi.org/10.1093/jxb/er... PMid:16364948.