Skip to main content
Log in

Bicarbonate use and carbon dioxide concentrating mechanisms in photosynthetic organisms

  • Short Communication
  • Published:
Acta Geochimica Aims and scope Submit manuscript

Abstract

Photosynthesis is crucial to the reduction of carbon dioxide in the atmosphere. The key enzyme of photosynthesis, Ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), has two mutably competing substrates, CO2 and O2. It has features of carboxylase and oxygenase. Rubisco performs the function of carboxylase to reduce inorganic carbon to form organic substances, which precondition is that more carbon dioxide accumulates around it. Carbon dioxide concentrating mechanisms (CCMs) are vital to cope with the limit of carbon dioxide. Various bicarbonate use pathway has a differential contribution to inorganic carbon assimilation. Bicarbonate transport, extracellular bicarbonate dehydration, or H+-ATPase-driven bicarbonate uptake, which induced CCMs, can support a considerable share of photosynthesis in photosynthetic organisms. However, CCMs in thylakoid membranes may be the most important. The CCMs occurred in the plasma membrane were secondary, evolutionary, and inducible, while CCMs coupled with photosynthetic oxygen evolution in thylakoid membranes, were primitive, major, and indispensable. A hypothetical schematic model of CCMs occurred in the plasma membrane and thylakoid membranes being proposed.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

References

  • Axelsson L, Larsson C, Ryberg H (1999) Affinity, capacity and oxygen sensitivity of two different mechanisms for bicarbonate utilization in Ulva lactuca L. (Chlorophyta). Plant Cell Environ 22(8): 969–978

  • Burnell OW, Connell SD, Irving AD, Watling JR, Russell BD (2014) Contemporary reliance on bicarbonate acquisition predicts increased growth of seagrass Amphibolis antarctica in a high-CO2 world. Conserv Physiol 2(1):cou052

    Article  Google Scholar 

  • Cabantchik ZI, Greger R (1992) Chemical probes for anion transporters of mammalian cell membranes. Am J Physiol-Cell Ph 262(4):C803–C827

    Article  Google Scholar 

  • Campbell JE, Fourqurean JW (2013) Mechanisms of bicarbonate use influence the photosynthetic carbon dioxide sensitivity of tropical seagrasses. Limnol Oceanogr 58(3):839–848

    Article  Google Scholar 

  • Charlotte P, Fernández J, Lourdes R, Pérez L, Terés J, Barceló J (2018) Transport and use of bicarbonate in plants: current knowledge and challenges ahead. Int J Mol Sci 19(5):1352

    Article  Google Scholar 

  • Choo K, Snoeijs P, Pedersen M (2002) Uptake of inorganic carbon by Cladophora glomerata (Chlorophyta) from the Baltic sea. J Phycol 38(3):493–502

    Article  Google Scholar 

  • Drobnitch ST, Nickols K, Edwards M (2016) Abiotic influences on bicarbonate use in the giant kelp, Macrocystis pyrifera, in the Monterey Bay. J Phycol 53(1):85–94

    Article  Google Scholar 

  • Fernández PA, Hurd CL, Roleda MY (2014) Bicarbonate uptake via an anion exchange protein is the main mechanism of inorganic carbon acquisition by the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae) under variable pH. J Phycol 50(6):998–1008

    Article  Google Scholar 

  • Gao KS, Zou DH (2001) Photosynthetic bicarbonate utilization by a terrestrial cyanobacterium, Nostoc flagelliforme (Cyanophyceae). J Phycol 37(5):768–771

    Article  Google Scholar 

  • Holland DP, Pantorno A, Orr PT, Stojkovic S, Beardall J (2012) The impacts of a high CO2 environment on a bicarbonate user: the cyanobacterium Cylindrospermopsis raciborskii. Water Res 46(5):1430–1437

    Article  Google Scholar 

  • Huertas IE, Espie GS, Colman B, Lubian LM (2000) Light-dependent bicarbonate uptake and CO2 efflux in the marine microalga Nannochloropsis gaditana. Planta 211(1):43–49

    Article  Google Scholar 

  • Hussner A, Mettler-Altmann T, Weber APM, Sand-Jensen K (2016) Acclimation of photosynthesis to supersaturated CO2 in aquatic plant bicarbonate users. Freshwater Biol 61(10):1720–1732

    Article  Google Scholar 

  • Ignatova LK, Rudenko NN, Khristin MS, Ivanov BN (2006) Heterogeneous origin of carbonic anhydrase activity of thylakoid membranes. Biochemistry-Moscow 71:525–532

    Article  Google Scholar 

  • Invers O, Zimmerman RC, Alberte RS, Pérez M, Romero J (2001) Inorganic carbon sources for seagrass photosynthesis: an experimental evaluation of bicarbonate use in species inhabiting temperate waters. J Exp Mar Biol Ecol 265(2):203–217

    Article  Google Scholar 

  • Jones JI (2005) The metabolic cost of bicarbonate use in the submerged plant Elodea nuttallii. Aquat Bot 83(1):71–81

    Article  Google Scholar 

  • Kaplan A, Zenvirth D, Reinhold L, Berry JA (1982) Involvement of a primary electrogenic pump in the mechanism for HCO3- uptake by the cyanobacterium Anabaena variabilis. Plant Physiol 69:978–982

    Article  Google Scholar 

  • Klenell M, Snoeijs P, Pedersen M (2004) Active carbon uptake in Laminaria digitata and L. saccharina (Phaeophyta) is driven by a proton pump in the plasma membrane. Hydrobiologia 514:41–53

    Article  Google Scholar 

  • Larsson C, Axelsson L (1999) Bicarbonate uptake and utilization in marine macroalgae. Eur J Phycol 34(1):79–86

    Article  Google Scholar 

  • Larsson C, Axelsson L, Ryberg H, Beer S (1997) Photosynthetic carbon utilization by Enteromorpha intestinalis (Chlorophyta) from a Swedish rockpool. Eur J Phycol 32(1):49–54

    Article  Google Scholar 

  • Maberly SC (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J Phycol 26:439–449

    Article  Google Scholar 

  • Moroney JV, Tolbert NE (1985) Inorganic carbon uptake by Chlamydomonas reinhardtii. Plant Physiol 77(2):253–258

    Article  Google Scholar 

  • Ow YX, Uthicke S, Collier CJ (2016) Light levels affect carbon utilisation in tropical seagrass under ocean acidification. PLoS ONE 11(3):e0150352

    Article  Google Scholar 

  • Roleda MY, Hurd CL (2012) Seaweed responses to ocean acidification. In: Wiencke C, Bischof K (eds) Seaweed Biology Ecological studies 219. Springer, Berlin

    Google Scholar 

  • Shitov AV, Pobeguts OV, Smolova TN, Allakhverdiev SI, Klimov VV (2009) Manganese-dependent carboanhydrase activity of photosystem II proteins. Biochemistry-Moscow 74(5):509–517

    Article  Google Scholar 

  • Shitov AV, Zharmukhamedov SK, Shutova TV, Allakhverdiev SI, Samuelsson G, Klimov VV (2011) A carbonic anhydrase inhibitor induces bicarbonate-reversible suppression of electron transfer in pea photosystem 2 membrane fragments. J Photoch Photobio B 104(1–2):366–371

    Article  Google Scholar 

  • Snoeijs P, Klenell M, Choo KS, Comhaire I, Ray S, Pedersén M (2002) Strategies for carbon acquisition in the red marine macroalga Coccotylus truncatus from the Baltic Sea. Mar Biol 140(3):435–444

    Article  Google Scholar 

  • Spalding MH (2008) Microalgal carbon-dioxide-concentrating mechanisms: chlamydomonas inorganic carbon transporters. J Exp Bot 59(7):1463–1473

    Article  Google Scholar 

  • Sültemeyer D (1998) Carbonic anhydrase in eukaryotic algae: characterization, regulation, and possible function during photosynthesis. Can J Bot 76(6):962–972

    Google Scholar 

  • Thielmann J, Tolber NE, Goyal A, Senger H (1990) Two systems for concentrating CO2 and bicarbonate during photosynthesis by Scenedesmus. Plant Physiol 92:622–629

    Article  Google Scholar 

  • Uehara S, Adachi F, Ito-Inaba Y, Inaba T (2016) Specific and efficient targeting of cyanobacterial bicarbonate transporters to the inner envelope membrane of chloroplasts in Arabidopsis. Front Plant Sci 7:16

    Article  Google Scholar 

  • Wang Y, Spalding MH (2014) Acclimation to very low CO2: contribution of limiting CO2 inducible proteins, LCIB and LCIA, to inorganic carbon uptake in Chlamydomonas reinhardtii. Plant Physiol 166(4):2040–2050

    Article  Google Scholar 

  • Wang Y, Duanmu D, Spalding MH (2011) Carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii: inorganic carbon transport and CO2 recapture. Photosynth Res 109(1–3):115–122

    Article  Google Scholar 

  • Wu Y (2021) Is bicarbonate directly used as substrate to participate in photosynthetic oxygen evolution. Acta Geochim. https://doi.org/10.1007/s11631-021-00484-0

    Article  Google Scholar 

  • Wu YY, Li HT, Xie TX (2015) The regulation on carbon source and carbon sequestration by microalgal carbonic anhydrase. Biogeochemical action of microalgal carbonic anhydrase. Science Press, Beijing, pp 76–111

    Google Scholar 

  • Yamano T, Sato E, Iguchi H, Fukuda Y, Fukuzawa H (2015) Characterization of cooperative bicarbonate uptake into chloroplast stroma in the green alga Chlamydomonas reinhardtii. P Natl Acad Sci USA 112(23):7315–7320

    Article  Google Scholar 

  • Young E, Beardall J, Giordano M (2001) Inorganic carbon acquisition by Dunaliella tertiolecta (Chlorophyta) involves external carbonic anhydrase and direct HCO3- utilization insensitive to the anion exchange inhibitor DIDS. Eur J Phycol 36(01):81–88

    Google Scholar 

  • Zoccola D, Ganot P, Bertucci A, Caminiti-Segonds N, Techer N, Voolstra CR, Aranda M, Tambutté E, Allemand D, Casey JR, Tambutté S (2015) Bicarbonate transporters in corals point towards a key step in the evolution of cnidarian calcification. Sci Rep 5(1):9983

    Article  Google Scholar 

  • Zou D, Gao K (2010) Acquisition of inorganic carbon by Endarachne binghamiae (Scytosiphonales, Phaeophyceae). Eur J Phycol 45(1):119–128

    Article  Google Scholar 

  • Zou D, Gao K, Xia J (2003) Photosynthetic utilization of inorganic carbon in the economic brown alga, Hizikia fusiforme (Sargassaceae) from the south china sea. J Phycol 39:1095–1100

    Article  Google Scholar 

  • Zweng RC, Koch MS, Bowes G (2018) The role of irradiance and C-use strategies in tropical macroalgae photosynthetic response to ocean acidification. Sci Rep 8(1):9479

    Article  Google Scholar 

Download references

Acknowledgements

The author thanks the foundations of the National Natural Science Foundation of China [No. U1612441-2], the National Key Research and Development Program of China [2016YFC0502602], and Support Plan Projects of Science and Technology Department of Guizhou Province [No. (2021)YB453].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yanyou Wu.

Ethics declarations

Conflict of interest

The author declares that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, Y. Bicarbonate use and carbon dioxide concentrating mechanisms in photosynthetic organisms. Acta Geochim 40, 846–853 (2021). https://doi.org/10.1007/s11631-021-00488-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11631-021-00488-w

Keywords

Navigation