Skip to main content
SpringerLink
Log in

Crosstalk between photosynthesis and respiration in microbes

  • Review
  • Published:
Journal of Biosciences Aims and scope Submit manuscript

Abstract

Phototrophic organisms harbor two main bioenergetic hubs, photosynthesis and respiration, and these processes dynamically exchange and share metabolites to balance the energy of the cell. In microalgae and cyanobacteria, the crosstalk between the light-triggered reactions of photosynthesis and respiration is particularly prominent with respiratory O2 uptake which can be stimulated upon illumination. Since its discovery, this light-enhanced respiration has been proposed to be critical in dissipating the excess reducing power generated by photosynthesis. Importantly, the physiological role and putative molecular mechanism involved have just recently started to be understood. Here, we revisit the physiological functions and discuss possible molecular mechanisms of interactions between the photosynthetic and respiratory electron flows in microalgae and cyanobacteria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1

Similar content being viewed by others

References

  • Bailleul B, Berne N, Murik O, et al. 2015 Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms. Nature 524 366–369

    Article  CAS  PubMed  ADS  Google Scholar 

  • Binder A 1982 Respiration and photosynthesis in energy-transducing membranes of cyanobacteria. J. Bioenerg. Biomembr. 14 271–286

    Article  CAS  PubMed  Google Scholar 

  • Bolychevtseva YV, Kuzminov FI, Elanskaya IV, et al. 2015 Photosystem activity and state transitions of the photosynthetic apparatus in cyanobacterium Synechocystis PCC 6803 mutants with different redox state of the plastoquinone pool. Biochemistry 80 50–60

    CAS  PubMed  Google Scholar 

  • Broddrick JT, Du N, Smith SR, et al. 2019 Cross-compartment metabolic coupling enables flexible photoprotective mechanisms in the diatom Phaeodactylum tricornutum. New Phytol. 222 1364–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burlacot A and Peltier G 2023 Energy crosstalk between photosynthesis and the algal CO2-concentrating mechanisms. Trends Plant Sci. 28 795–807

    Article  CAS  PubMed  Google Scholar 

  • Burlacot A, Dao O, Auroy P, et al. 2022 Alternative photosynthesis pathways drive the algal CO2-concentrating mechanism. Nature 605 366–371

    Article  CAS  PubMed  ADS  Google Scholar 

  • Cardol P, Gloire G, Havaux M, et al. 2003 Photosynthesis and state transitions in mitochondrial mutants of Chlamydomonas reinhardtii affected in respiration. Plant Physiol. 133 2010–2020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardol P, Alric J, Girard-Bascou J, et al. 2009 Impaired respiration discloses the physiological significance of state transitions in Chlamydomonas. Proc. Natl. Acad. Sci. USA 106 15979–15984

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Dao O, Kuhnert F, Weber APM, et al. 2022 Physiological functions of malate shuttles in plants and algae. Trends Plant Sci. 27 488–501

    Article  CAS  PubMed  Google Scholar 

  • Ekelund NGA 2000 Interactions between photosynthesis and ‘light-enhanced dark respiration’ (LEDR) in the flagellate Euglena gracilis after irradiation with ultraviolet radiation. J. Photochem. Photobiol. B Biol. 55 63–69

    Article  CAS  Google Scholar 

  • Fisher NL, Campbell DA, Hughes DJ, et al. 2021 Divergence of photosynthetic strategies amongst marine diatoms. PLoS One 15 e0244252

    Article  Google Scholar 

  • Hatano J, Kusama S, Tanaka K, et al. 2022 NADPH production in dark stages is critical for cyanobacterial photocurrent generation: a study using mutants deficient in oxidative pentose phosphate pathway. Photosynth. Res. 153 113–120

    Article  CAS  PubMed  Google Scholar 

  • Hirano M, Satoh K and Katoh S 1980 Plastoquinone as a common link between photosynthesis and respiration in a blue-green alga. Photosynth. Res. 1 149–162

    Article  CAS  PubMed  Google Scholar 

  • Huang W, Krishnan A, Plett A, et al. 2023 Chlamydomonas mutants lacking chloroplast TRIOSE PHOSPHATE TRANSPORTER3 are metabolically compromised and light sensitive. Plant Cell 35 2592–2614

    Article  PubMed  Google Scholar 

  • Kaye Y, Huang W, Clowez S, et al. 2019 The mitochondrial alternative oxidase from Chlamydomonas reinhardtii enables survival in high light. J. Biol. Chem. 294 1380–1395

    Article  CAS  PubMed  Google Scholar 

  • Kramer DM and Evans JR 2011 The importance of energy balance in improving photosynthetic productivity. Plant Physiol. 155 70–78

    Article  CAS  PubMed  Google Scholar 

  • Krieger-Liszkay A and Shimakawa G 2022 Regulation of the generation of reactive oxygen species during photosynthetic electron transport. Biochem. Soc. Trans. 50 1025–1034

    Article  CAS  PubMed  Google Scholar 

  • Lemaire C, Wollman FA and Bennoun P 1988 Restoration of phototrophic growth in a mutant of Chlamydomonas reinhardtii in which the chloroplast atpB gene of the ATP synthase has a deletion: an example of mitochondria-dependent photosynthesis. Proc. Natl. Acad. Sci. USA 85 1344–1348

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Levering J, Broddrick J, Dupont CL, et al. 2016 Genome-scale model reveals metabolic basis of biomass partitioning in a model diatom. PLoS One 11 e0155038

    Article  PubMed  PubMed Central  Google Scholar 

  • McCashin BG, Cossins EA and Canvin DT 1988 Dark respiration during photosynthesis in wheat leaf slices. Plant Physiol. 87 155–161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Misumi M, Katoh H, Tomo T, et al. 2016 Relationship between photochemical quenching and non-photochemical quenching in six species of cyanobacteria reveals species difference in redox state and species commonality in energy dissipation. Plant Cell Physiol. 57 1510–1517

    CAS  PubMed  Google Scholar 

  • Moog D, Rensing SA, Archibald JM, et al. 2015 Localization and evolution of putative triose phosphate translocators in the diatom Phaeodactylum tricornutum. Genome Biol. Evol. 7 2955–2969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murik O, Tirichine L, Prihoda J, et al. 2019 Downregulation of mitochondrial alternative oxidase affects chloroplast function, redox status and stress response in a marine diatom. New Phytol. 221 1303–1316

    Article  CAS  PubMed  Google Scholar 

  • Noguchi K and Yoshida K 2008 Interaction between photosynthesis and respiration in illuminated leaves. Mitochondrion 8 87–99

    Article  CAS  PubMed  Google Scholar 

  • Nunes-Nesi A, Sweetlove LJ and Fernie AR 2007 Operation and function of the tricarboxylic acid cycle in the illuminated leaf. Physiol. Plant. 129 45–56

    Article  CAS  Google Scholar 

  • Ocheretina O, Haferkamp I, Tellioglu H, et al. 2000 Light-modulated NADP-malate dehydrogenases from mossfern and green algae: insights into evolution of the enzyme’s regulation. Gene 258 147–154

    Article  CAS  PubMed  Google Scholar 

  • Ogawa T, Suzuki K and Sonoike K 2021 Respiration interacts with photosynthesis through the acceptor side of photosystem I, reflected in the dark-to-light induction kinetics of chlorophyll fluorescence in the cyanobacterium Synechocystis sp. PCC 6803. Front. Plant Sci. 12 1556

    Article  Google Scholar 

  • Pelroy RA and Bassham JA 1972 Photosynthetic and dark carbon metabolism in unicellular blue-green algae. Archiv Mikrobiol. 86 25–38

    Article  CAS  Google Scholar 

  • Peltier G and Thibault P 1985 O2 uptake in the light in Chlamydomonas: Evidence for persistent mitochondrial respiration. Plant Physiol. 79 225–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peltier G, Stoffel C, Findinier J, et al. 2023 Algal CO2 capture is powered by alternative electron pathways of photosynthesis. bioRxiv https://doi.org/10.1101/2023.08.08.552514

  • Peschek GA, Obinger C and Paumann M 2004 The respiratory chain of blue-green algae (cyanobacteria). Physiol. Plant. 120 358–369

    Article  CAS  PubMed  Google Scholar 

  • Pierangelini M, Thiry M and Cardol P 2020 Different levels of energetic coupling between photosynthesis and respiration do not determine the occurrence of adaptive responses of Symbiodiniaceae to global warming. New Phytol. 228 855–868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pils D and Schmetterer G 2001 Characterization of three bioenergetically active respiratory terminal oxidases in the cyanobacterium Synechocystis sp. strain PCC 6803. FEMS Microbiol. Lett. 203 217–222

    Article  CAS  PubMed  Google Scholar 

  • Raghavendra AS and Padmasree K 2003 Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci. 8 546–553

    Article  CAS  PubMed  Google Scholar 

  • Shimakawa G 2023 Electron transport in cyanobacterial thylakoid membranes: are cyanobacteria simple models for photosynthetic organisms? J. Exp. Bot. 74 3476–3487

    Article  CAS  PubMed  Google Scholar 

  • Shimakawa G and Miyake C 2018 Respiratory terminal oxidases alleviate photo-oxidative damage in photosystem I during repetitive short-pulse illumination in Synechocystis sp. PCC 6803. Photosynth. Res. 137 241–250

    Article  CAS  PubMed  Google Scholar 

  • Shimakawa G, Hasunuma T, Kondo A, et al. 2014 Respiration accumulates Calvin cycle intermediates for the rapid start of photosynthesis in Synechocystis sp. PCC 6803. Biosci. Biotechnol. Biochem. 78 1997–2007

    Article  CAS  PubMed  Google Scholar 

  • Shimakawa G, Kohara A and Miyake C 2021 Characterization of light-enhanced respiration in cyanobacteria. Int. J. Mol. Sci. 22 342

    Article  CAS  Google Scholar 

  • Tanaka K, Shirai T, Vavricka CJ, et al. 2022 Dark accumulation of downstream glycolytic intermediates initiates robust photosynthesis in cyanobacteria. Plant Physiol. 191 2400–2413

    Article  PubMed Central  Google Scholar 

  • Viola S, Sellés J, Bailleul B, et al. 2021 In vivo electron donation from plastocyanin and cytochrome c6 to PSI in Synechocystis sp. PCC6803. Biochim. Biophys. Acta Bioenerg. 1862 148449

    Article  CAS  PubMed  Google Scholar 

  • Weger HG, Herzig R, Falkowski PG, et al. 1989 Respiratory losses in the light in a marine diatom: Measurements by short-term mass spectrometry. Limnol. Oceanogr. 34 1153–1161

    Article  CAS  ADS  Google Scholar 

  • Xue X, Gauthier DA, Turpin DH, et al. 1996 Interactions between photosynthesis and respiration in the green alga Chlamydomonas reinhardtii (characterization of light-enhanced dark respiration). Plant Physiol. 112 1005–1014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang C, Hua Q and Shimizu K 2002 Metabolic flux analysis in Synechocystis using isotope distribution from 13C-labeled glucose. Metab. Eng. 4 202–216

    Article  CAS  PubMed  Google Scholar 

  • Yokochi Y, Yoshida K, Hahn F, et al. 2021 Redox regulation of NADP-malate dehydrogenase is vital for land plants under fluctuating light environment. Proc. Natl. Acad. Sci. USA 118 e2016903118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the Japan Society for the Promotion of Science (JSPS; grant no. 21K15122 to GS) and by the Carnegie Institution for Science (AB).

Author information

Authors and Affiliations

  1. Department of Bioscience, School of Biological and Environmental Sciences, Kwansei-Gakuin University, 1 Gakuen Uegahara, Sanda, Hyogo, 669-1330, Japan

    Ginga Shimakawa & Yusuke Matsuda

  2. Department of Plant Biology, The Carnegie Institution for Science, Stanford, CA, 94305, USA

    Adrien Burlacot

  3. Department of Biology, Stanford University, Stanford, CA, 94305, USA

    Adrien Burlacot

Authors
  1. Ginga Shimakawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yusuke Matsuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adrien Burlacot
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors wrote the manuscript.

Corresponding authors

Correspondence to Ginga Shimakawa or Adrien Burlacot.

Ethics declarations

Conflict of interest

The authors have no conflict of interest to declare.

Additional information

Corresponding editor: Ko Noguchi

This article is part of the Topical Collection: Plant Mitochondria: Properties and Interactions with Other Organelles.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shimakawa, G., Matsuda, Y. & Burlacot, A. Crosstalk between photosynthesis and respiration in microbes. J Biosci 49, 45 (2024). https://doi.org/10.1007/s12038-023-00417-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12038-023-00417-4

Keywords

Search

Navigation