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.
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
Cabantchik ZI, Greger R (1992) Chemical probes for anion transporters of mammalian cell membranes. Am J Physiol-Cell Ph 262(4):C803–C827
Campbell JE, Fourqurean JW (2013) Mechanisms of bicarbonate use influence the photosynthetic carbon dioxide sensitivity of tropical seagrasses. Limnol Oceanogr 58(3):839–848
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
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
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
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
Gao KS, Zou DH (2001) Photosynthetic bicarbonate utilization by a terrestrial cyanobacterium, Nostoc flagelliforme (Cyanophyceae). J Phycol 37(5):768–771
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
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
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
Ignatova LK, Rudenko NN, Khristin MS, Ivanov BN (2006) Heterogeneous origin of carbonic anhydrase activity of thylakoid membranes. Biochemistry-Moscow 71:525–532
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
Jones JI (2005) The metabolic cost of bicarbonate use in the submerged plant Elodea nuttallii. Aquat Bot 83(1):71–81
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
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
Larsson C, Axelsson L (1999) Bicarbonate uptake and utilization in marine macroalgae. Eur J Phycol 34(1):79–86
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
Maberly SC (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J Phycol 26:439–449
Moroney JV, Tolbert NE (1985) Inorganic carbon uptake by Chlamydomonas reinhardtii. Plant Physiol 77(2):253–258
Ow YX, Uthicke S, Collier CJ (2016) Light levels affect carbon utilisation in tropical seagrass under ocean acidification. PLoS ONE 11(3):e0150352
Roleda MY, Hurd CL (2012) Seaweed responses to ocean acidification. In: Wiencke C, Bischof K (eds) Seaweed Biology Ecological studies 219. Springer, Berlin
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
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
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
Spalding MH (2008) Microalgal carbon-dioxide-concentrating mechanisms: chlamydomonas inorganic carbon transporters. J Exp Bot 59(7):1463–1473
Sültemeyer D (1998) Carbonic anhydrase in eukaryotic algae: characterization, regulation, and possible function during photosynthesis. Can J Bot 76(6):962–972
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
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
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
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
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
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
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
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
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
Zou D, Gao K (2010) Acquisition of inorganic carbon by Endarachne binghamiae (Scytosiphonales, Phaeophyceae). Eur J Phycol 45(1):119–128
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
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
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
Corresponding author
Ethics declarations
Conflict of interest
The author declares that they have no conflict of interest.
Rights and permissions
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11631-021-00488-w