Utilization of HCO 3 − at high pH by the brown macroalga Laminaria saccharina

Axelsson, Lennart; Mercado, Jesús; Figueroa, Félix

doi:10.1080/09670260010001735621

Cited by 107Marine and coastal plant biologyMarine Plankton and BiogeochemistryAlgal biology and biofuel production

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Utilization of HCO 3 − at high pH by the brown macroalga Laminaria saccharina

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Axelsson, Lennart, Mercado, Jesús, Figueroa, Félix·2000·European Journal of Phycology

DOI 10.1080/09670260010001735621

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Abstract

The brown macroalga Laminaria saccharina exhibits a type of HCO3 − utilization that could be almost completely inhibited either by proton buffers or by acetazolamide, an inhibitor of extracellularly operating carbonic anhydrase. This means of HCO3 − utilization featured properties similar to direct HCO3 − uptake in that photosynthetic rates were proportional to the HCO3 − concentration of the seawater over a wide pH range (pH 7.0−9.5). Despite this, it must be characterized as carbonic anhydrase-catalysed external HCO3 − dehydration and not as direct HCO3 − uptake. A mechanism is suggested involving a CO2-concentrating capability located at the cell membrane. This mechanism, which might be common in brown algae, is suggested to have an adaptational advantage in colder regions of the sea (as compared with the direct HCO3 − uptake of green macroalgae). This means of HCO3 − utilization is inhibited even by fairly low concentrations of buffer, with consequences for the interpretation of earlier experimental studies on L. saccharina (and possibly other brown algae). These consequences relate both to ecology (e.g. determination of inorganic C affinity) and physiology (e.g. assessing mechanisms for inorganic C uptake).

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Light fuels the generation of ATP for both carbon fixation and HCO3- uptake.
“Light fuels the generation of ATP for both carbon fixation and HCO3- uptake [48, 58].”
From Light Levels Affect Carbon Utilisation in Tropical Seagrass under Ocean Acidification (2016) · cites this paper as [48]
The Discussion (page not provided) describes an energy-consuming process involved in HCO3− utilization. It does not say that light generates ATP for that process or for carbon fixation; it says the relationship between blue light and HCO3− acquisition remains under investigation. (LLM, conf=0.84)
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Klenell, M., Snoeijs, P. J. M., & Pedersén, M. (2004) · Springer eBooks · doi:10.1007/978-94-017-0920-0_4 · Cited by 46
Acclimation Responses of Gracilaria sp. (Rhodophyta) and Enteromorpha intestinalis (Chlorophyta) to Changes in the External Inorganic Carbon Concentration
Andría, J. R., Brun, F. G., Pérez‐Lloréns, J. L., & Vergara, J. J. (2001) · Botanica Marina · doi:10.1515/bot.2001.046 · Cited by 43
“…microalgae such as Chlamydomonas reinhardtii Dangeard by Sültemeyer et al. 1989) and facilitated CO2 entry in acidic regions of the cell membrane (Lucas 1983, Price and Badger 1985, Björk et al. 1992, Axelsson et al. 2000), both mechanisms may or may not be associated with the external CA activity.”
Background
Different mechanisms of inorganic carbon acquisition in red macroalgae (Rhodophyta) revealed by the use of TRIS buffer
Moulin, P., Andría, J. R., Axelsson, L., & Mercado, J. M. (2011) · Aquatic Botany · doi:10.1016/j.aquabot.2011.03.007 · Cited by 42
Self-citation
Effects of secular variation in seawater Mg/Ca ratio (calcite–aragonite seas) on CaCO3 sediment production by the calcareous algae Halimeda, Penicillus and Udotea– evidence from recent experiments and the geological record
Ries, J. B. (2009) · Terra Nova · doi:10.1111/j.1365-3121.2009.00899.x · Cited by 41
“…algae through the intracellular extraction of CO2 from HCO3 ) by the enzyme carbonic anhydrase, which liberates OH- that is extruded into the algae s interutricular fluid (Borowitzka and Larkum, 1976b; Axelsson et al., 2000; Hellblom et al., 2001; Hellblom and Axelsson, 2003; Uku et al., 2005).”
Background
Modeling the growth of sugar kelp (Saccharina latissima) in aquaculture systems using dynamic energy budget theory.
Venolia, C. T., Lavaud, R., Green-Gavrielidis, L. A., Thornber, C., & Humphries, A. T. (2020) · Ecological Modelling · doi:10.1016/j.ecolmodel.2020.109151 · Cited by 40
“On the C side of the model, since S. latissima and other algae use carbonic anhydrase to assimilate bicarbonate and convert it into carbon dioxide (Axelsson et al., 2000), we assumed that assimilating carbon dioxide directly was identical to assimilating carbon dioxide that was formed…”
Background
Effects of Shellfish and Macro-Algae IMTA in North China on the Environment, Inorganic Carbon System, Organic Carbon System, and Sea–Air CO2 Fluxes
Liu, Y., Zhang, J., Wu, W., Zhong, Y., Li, H., Wang, X., Yang, J., & Zhang, Y. (2022) · Frontiers in Marine Science · doi:10.3389/fmars.2022.864306 · Cited by 40
“Macro-algae uses bicarbonate ions as an external carbon source for photosynthesis, ingests a large amount of DIC during growth, and affects the pCO2 and TA in surface seawater (Axelsson et al., 2000).”
Background
Increased temperature and CO2 alleviate photoinhibition in Desmarestia anceps: from transcriptomics to carbon utilization
Íñiguez, C., Heinrich, S., Harms, L., & Gordillo, F. J. L. (2017) · Journal of Experimental Botany · doi:10.1093/jxb/erx164 · Cited by 39
“Similar results have been observed in previous studies with some members of the family Laminariaceae (Giordano and Maberly, 1989; Surif and Raven, 1989), whose CCMs are based on the simultaneous operation of proton pumps and periplasmic CA activity (Axelsson et al., 2000; Klenell et al., 2004).”
Result
Influence of Seaweed Aquaculture on Marine Inorganic Carbon Dynamics and Sea‐air CO 2 Flux
Jiang, Z., Fang, J., Mao, Y., Han, T., & Wang, G. (2013) · Journal of the World Aquaculture Society · doi:10.1111/jwas.12000 · Cited by 38
Acquisition and metabolism of carbon in the Ochrophyta other than diatoms
Raven, J. A., & Giordano, M. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0400 · Cited by 39
Effects of pH on the growth rate, motility and photosynthesis inEuglena gracilis
Danilov, R. A., & Ekelund, N. (2001) · Folia Microbiologica · doi:10.1007/bf02818001 · Cited by 37
Inorganic carbon acquisition in algal communities: are the laboratory data relevant to the natural ecosystems?
Mercado, J. M., & Gordillo, F. J. L. (2011) · Photosynthesis Research · doi:10.1007/s11120-011-9646-0 · Cited by 38
Self-citation
Use of light and inorganic carbon acquisition by two morphotypes of Zostera noltii Hornem
Mercado, J. M., Niell, F. X., Silva, J., & Santos, R. (2003) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/s0022-0981(03)00368-x · Cited by 36
“The effect of Tris buffer on photosynthesis was tested at pH 8.2 as described by Axelsson et al. (2000), prior to testing the effect of the inhibitors of carbonic anhydrase (CA) on oxygen evolution.”
BackgroundMethodInfluentialSelf-citation
Evidence for a plasmalemma-based CO2 concentrating mechanism in Laminaria saccharina
Mercado, J. M., Andría, J. R., Pérez‐Lloréns, J. L., Vergara, J. J., & Axelsson, L. (2006) · Photosynthesis Research · doi:10.1007/s11120-006-9039-y · Cited by 32
Self-citation
Light Levels Affect Carbon Utilisation in Tropical Seagrass under Ocean Acidification
Ow, Y. X., Uthicke, S., & Collier, C. J. (2016) · PLOS ONE · doi:10.1371/journal.pone.0150352 · Cited by 31
“Light fuels the generation of ATP for both carbon fixation and HCO3 - uptake [48, 58].”
Background
Carbon Limitation
Axelsson, L., & Beer, S. (2001) · Springer eBooks · doi:10.1007/978-3-642-59491-5_2 · Cited by 31
Self-citation
Divergent responses in growth and nutritional quality of coastal macroalgae to the combination of increased pCO2 and nutrients
Ober, G. T., & Thornber, C. (2017) · Marine Environmental Research · doi:10.1016/j.marenvres.2017.09.003 · Cited by 32
“By contrast, we predicted that extreme levels of pCO 2 will decrease the growth rate of Fucus , which is likely to occur due to potential pH sensitivity of its CCM (Axelsson et al., 2000; Gutow et al., 2014), but increase tissue quality (as seen in Gutow et al., 2014).”
BackgroundInfluential
The role of Gracilaria lemaneiformis in eliminating the dissolved inorganic carbon released from calcification and respiration process of Chlamys farreri
Jiang, Z. J., Fang, J. G., Han, T. T., Mao, Y. Z., Li, J. Q., & Du, M. R. (2013) · Journal of Applied Phycology · doi:10.1007/s10811-013-0110-8 · Cited by 31
“Previous studies have showed that a number of marine seaweeds , such as Laminaria saccharina (Axelsson et al. 2000), Gracilaria gaditana (Andria et al. 1999), Ulva lactuca (Maberly et al. 1992), Porphyra haitanensis (Zou et al. 2002), and Porphyra linearis (Israel et al. 1999) were able to use HCO…”
Background
Characterization of α-type carbonic anhydrase (CA) gene and subcellular localization of α-CA in the gametophytes of Saccharina japonica
Ye, R.-X., Yu, Z., Shi, W., Gao, H.-J., Bi, Y.-H., & Zhou, Z. (2013) · Journal of Applied Phycology · doi:10.1007/s10811-013-0221-2 · Cited by 30
“SjCA transcription levels under different carbon resources The gametophytes were cultivated in mediumwith filtered air, filtered air+3 % CO2 and 0.018 M NaHCO3 independently, and were collected at 00:00, 08:00, 16:00, and 24:00 hours, and the number of replicates was 3.”
BackgroundInfluential
Ecosystem Metabolism Modulates the Dynamics of Hypoxia and Acidification Across Temperate Coastal Habitat Types
Wallace, R. B., Peterson, B. J., & Gobler, C. J. (2021) · Frontiers in Marine Science · doi:10.3389/fmars.2021.611781 · Cited by 28
“Additionally, increased HCO3− uptake by macroalgae may have contributed to decreased TA via release of H+ by macroalgae via active extrusion pump as pHT in the surrounding water column reaches extreme levels (Uusitalo, 1996; Axelsson et al., 2000).”
Background
Effects of elevated nutrients and CO 2 emission scenarios on three coral reef macroalgae
Bender‐Champ, D., Díaz-Pulido, G., & Dove, S. (2017) · Harmful Algae · doi:10.1016/j.hal.2017.04.004 · Cited by 30
“The application of TRIS buffered at pH 9.7 led to negligible net photosynthetic O2 evolution, suggesting that proton efflux is important for facilitating the conversion of bicarbonate to CO2 at the external membrane in this species (Axelsson et al., 2000).”
BackgroundInfluential
Is the tetrasporophyte of Asparagopsis armata (Bonnemaisoniales) limited by inorganic carbon in integrated aquaculture?1
Mata, L. J., Silva, J., Schuenhoff, A., & Santos, R. (2007) · Journal of Phycology · doi:10.1111/j.1529-8817.2007.00421.x · Cited by 28
“Inhibitory effect of the Tris buffer was previously demonstrated for some marine plants (Axelsson et al. 2000, Mercado et al. 2003).”
Background
Strategies for carbon acquisition in the red marine macroalga Coccotylus truncatus from the Baltic Sea
Snoeijs, P. J. M., Klenell, M., Choo, K., Comhaire, I., Ray, S., & n, M. P. X. E. (2002) · Marine Biology · doi:10.1007/s00227-001-0729-x · Cited by 27
Effects of Seven Antifouling Compounds on Photosynthesis and Inorganic Carbon Use in Sugar Kelp Saccharina latissima (Linnaeus)
Johansson, P., Eriksson, K. M., Axelsson, L., & Blanck, H. (2012) · Archives of Environmental Contamination and Toxicology · doi:10.1007/s00244-012-9778-z · Cited by 25
Self-citation
Diverse responses of sporophytic photochemical efficiency and gametophytic growth for two edible kelps, Saccharina japonica and Undaria pinnatifida, to ocean acidification and warming
Gao, X., Kim, J., Park, S. K., Yu, O. H., Kim, Y. S., & Choi, H. G. (2019) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2019.03.063 · Cited by 24
Seasonal and tidal variability of environmental carbon related physico-chemical variables and inorganic C acquisition in Gracilariopsis longissima and Enteromorpha intestinalis from Los Toruños salt marsh (Cádiz Bay, Spain)
Pérez‐Lloréns, J. L., Brun, F. G., Andría, J. R., & Vergara, J. J. (2004) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2003.12.003 · Cited by 24
THE INVOLVEMENT OF A PLASMA MEMBRANE H+‐ATPase IN THE BLUE‐LIGHT ENHANCEMENT OF PHOTOSYNTHESIS IN LAMINARIA DIGITATA (PHAEOPHYTA)1
Klenell, M., Snoeijs, P. J. M., & Pedersén, M. (2002) · Journal of Phycology · doi:10.1046/j.1529-8817.2002.02063.x · Cited by 22
“This is consistent with the results of Axelsson et al. (2000) that HCO3 utilization in Laminaria saccharina is strongly inhibited by 50 mM Tris, which would dissipate the acid zones.”
Result
Photosynthetic bicarbonate utilization in Porphyra haitanen-sis (Bangiales, Rhodophyta)
Zou, D., & Gao, K. (2002) · Chinese Science Bulletin · doi:10.1360/02tb9358 · Cited by 29
The impact of CO2 emission scenarios and nutrient enrichment on a common coral reef macroalga is modified by temporal effects
Bender‐Champ, D., Díaz-Pulido, G., & Dove, S. (2013) · Journal of Phycology · doi:10.1111/jpy.12153 · Cited by 21
“…(CCM) involving either direct HCO3 uptake, or uptake of CO2 following conversion from HCO3 by an external carbonic anhydrase (CA), to ultimately increase CO2 concentration at the site of fixation (Surif and Raven 1989, Maberly 1990, Badger et al. 1998, Axelsson et al. 2000, Raven and Hurd 2012).”
Background
Deleterious effect of TRIS buffer on growth rates and pigment content of Gracilaria birdiae Plastino & E.C. Oliveira (Gracilariales, Rhodophyta)
Ursi, S., Guimarães, M., & Plastino, E. M. (2008) · Acta Botanica Brasilica · doi:10.1590/s0102-33062008000300024 · Cited by 21
“…that TRIS has a deleterious effect on photosynthesis by inhibition of mechanisms such as the transport of HCO3 - across the plasma membrane (Axelsson et al. 2000; Hellblom et al. 2001) or O 2 evolution in Photosystem II (Sofrová et al. 1978; Rickert et al. 1991; Jegerschold & Styring 1996).”
Photosynthetic carbon acquisition in Sargassum henslowianum (Fucales, Phaeophyta), with special reference to the comparison between the vegetative and reproductive tissues
Zou, D., Gao, K., & Chen, W. (2011) · Photosynthesis Research · doi:10.1007/s11120-010-9612-2 · Cited by 19
“CO2?”
BackgroundInfluential
Effect of Tris-(hydroxymethyl)-amino methane on microalgae biomass growth in a photobioreactor
Nguyen, T.-T., Bui, X., Pham, D. M., Guo, W., & Ngo, H. H. (2016) · Bioresource Technology · doi:10.1016/j.biortech.2016.02.043 · Cited by 19
“83 Previous studies have indicated that Tris impacts on photosynthesis by inhibiting 84 mechanisms such as the transportation of HCO3 - across the plasma membrane 85 (Axelsson et al., 2000).”
Background
Kelps and Environmental Changes in Kongsfjorden: Stress Perception and Responses
Bischof, K., Buschbaum, C., Fredriksen, S., Gordillo, F. J. L., Heinrich, S., Jiménez, C., Lütz, C., Molis, M., Roleda, M. Y., Schwanitz, M., et al. (2019) · Advances in polar ecology · doi:10.1007/978-3-319-46425-1_10 · Cited by 18
Acquisition of inorganic carbon by Endarachne binghamiae (Scytosiphonales, Phaeophyceae)
Zou, D., & Gao, K. (2010) · European Journal of Phycology · doi:10.1080/09670260903383909 · Cited by 18
“However, it has been demonstrated that the buffers per se could inhibit the photosynthetic carbon acquisition in the marine brown seaweed, Saccharina latissima (Axelsson et al., 2000; Mercado et al., 2006) and in the seagrass Zostera marina (Hellblom et al., 2001).”
BackgroundInfluential
Diversity of CO2 Concentrating Mechanisms in Macroalgae Photosynthesis: A Case Study of Ulva sp.
Sun, J., Zhao, C., Zhao, S., Dai, W., Liu, J., Zhang, J., Xu, J., & He, P. (2023) · Journal of Marine Science and Engineering · doi:10.3390/jmse11101911 · Cited by 18
Photosynthetic Utilization of Bicarbonate in Zostera marina Is Reduced by Inhibitors of Mitochondrial ATPase and Electron Transport
Carr, H., & Axelsson, L. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.107.115584 · Cited by 16
Self-citation
Photosynthetic inorganic carbon utilization of gametophytes and sporophytes of Undaria pinnatifida (Phaeophyceae)
Zhang, X., Hu, H., & Tan, T. (2006) · Phycologia · doi:10.2216/05-28.1 · Cited by 16
“The ability of using HCO3 by means of this mechanism is generally reduced sharply by increased pH, and is essentially very poor at above pH 9.5 (Axelsson et al. 1995, 2000).”
BackgroundInfluential
Sporophytic photosynthesis and gametophytic growth of the kelp Ecklonia stolonifera affected by ocean acidification and warming
Gao, X., Choi, H. G., Park, S. K., Kim, J., Yu, O. H., & Nam, K. W. (2019) · Aquaculture Research · doi:10.1111/are.13957 · Cited by 14
Mechanisms of Ion Transport in Halophytes: From Roots to Leaves
Volkov, V. S., & Flowers, T. J. (2019) · Tasks for vegetation science · doi:10.1007/978-3-030-04417-6_10 · Cited by 14
The Brown Algae Saccharina japonica and Sargassum horneri Exhibit Species-Specific Responses to Synergistic Stress of Ocean Acidification and Eutrophication
Liu, Y., Cao, J., Chu, Y., Liu, Y., Wang, Q., Gong, Q., & Li, J. (2021) · Journal of Ocean University of China · doi:10.1007/s11802-021-4853-6 · Cited by 14
Absorption and Transport of Inorganic Carbon in Kelps with Emphasis on Saccharina japonica
Bi, Y., & Zhou, Z. (2016) · InTech eBooks · doi:10.5772/62297 · Cited by 12
“In seawater, the dominant species of Ci is HCO3 [11].”
Background
Effects of inorganic carbon concentration and pH on carbonic anhydrase activity of gametophytes of Saccharina japonica
Bi, Y., Liang, C.-L., Li, J.-L., Yin, H., Tian, R.-T., & Zhou, Z.-G. (2020) · Aquaculture and Fisheries · doi:10.1016/j.aaf.2020.01.003 · Cited by 12
Identification and Characterization of a Periplasmic α‐Carbonic Anhydrase (CA) in the Gametophytes of Saccharina japonica (Phaeophyceae)
Bi, Y., Qiao, Y., Wang, Z., & Zhou, Z. (2020) · Journal of Phycology · doi:10.1111/jpy.13091 · Cited by 12
Water motion and pH jointly impact the availability of dissolved inorganic carbon to macroalgae
James, R. K., Hepburn, C. D., Pritchard, D. W., Richards, D. K., & Hurd, C. L. (2022) · Scientific Reports · doi:10.1038/s41598-022-26517-z · Cited by 13
Photosynthetic use of inorganic carbon in deep-water kelps from the Strait of Gibraltar
García‐Sánchez, M. J., Delgado‐Huertas, A., Fernández, J. A., & Flores‐Moya, A. (2015) · Photosynthesis Research · doi:10.1007/s11120-015-0184-z · Cited by 11
The Interactive Effects of Elevated CO2 and Ammonium Enrichment on the Physiological Performances of Saccharina japonica (Laminariales, Phaeophyta)
Kang, J. W., & Chung, I. K. (2018) · Ocean Science Journal · doi:10.1007/s12601-018-0014-2 · Cited by 10
“Furthermore, at pH units below or over 9.0, Saccharina sp. could take up CO2 via external CA activity (Axelsson et al. 2000; Olischläger et al. 2012).”
BackgroundInfluential
Effects of Increasing Temperature and Ocean Acidification on the Microstages of two Populations of Saccharina latissima in the Northwest Atlantic
Redmond, S. (2013) · OpenCommons - UConn (University of Connecticut) · Cited by 9
Expression of a periplasmic β-carbonic anhydrase (CA) gene is positively correlated with HCO3- utilization by the gametophytes of Saccharina japonica (Phaeophyceae, Ochrophyta)
Hao, H.-M., Bi, Y., Wei, N.-N., Lin, P.-C., Mei, S.-H., & Zhou, Z. (2023) · Journal of Applied Phycology · doi:10.1007/s10811-023-03088-8 · Cited by 8
“Such a strategy for HCO 3-utilization has also been examined in the other Laminariales (Surif and Raven 1989; Haglund et al. 1992; Axelsson et al. 2000; García-Sánchez et al. 2016), suggesting that all could use exogenous HCO 3-for photosynthesis in the same manner.”
Method
The Influence of CO2 Enrichment on Net Photosynthesis of Seagrass Zostera marina in a Brackish Water Environment
Pajusalu, L., Martin, G., Põllumäe, A., & Paalme, T. (2016) · Frontiers in Marine Science · doi:10.3389/fmars.2016.00239 · Cited by 7
“Similarly, Axelsson et al. (2000) found that brown macroalgae Laminaria saccharina appears to be able to utilize the HCO−3 of seawater even more efficiently at high pH. Seagrass meadows are amongst the most productive autotrophic ecosystems on the planet (Duarte and Chiscano, 1999).”
Background
Inorganic Carbon Acquisition by Aquatic Primary Producers
Rokitta, S. D., Kranz, S. A., & Rost, B. (2022) · Wiley eBooks · doi:10.1002/9781119986782.ch4 · Cited by 7
Effects of increased pH and inorganic carbon on growth and photosynthesis in the macroalga Gracilaria lemaneiformis (Gigartinales, Rhodophyta)
Wang, L., Jiang, H., Zou, D., & Ye, C. (2020) · Phycologia · doi:10.1080/00318884.2020.1732716 · Cited by 7
“Accordingly, a combined effect of carbon limitation and pH restriction would limit photosynthesis of macroalgae (Axelsson et al. 2000; Raven & Beardall 2014).”
Background
Shellfish-macroalgae IMTA maintaining water environment stability: A case study of Crassostrea gigas and Gracilaria lemaneiformis IMTA in Sanggou Bay of China
Tong, R., Zhang, R., Fang, J., Zhang, Y., Xu, J., Zhang, X., & Xie, Y. (2025) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2025.117943 · Cited by 5
Photoautotrophic cultivation of Chlamydomonas reinhardtii in open ponds of greenhouse
Chandrashekharaiah, P. S., Paul, V., Kodgire, S., Chawada, H., Thorat, R., Kushwaha, S., Sanyal, D., & Dasgupta, S. (2021) · Archives of Microbiology · doi:10.1007/s00203-020-02124-2 · Cited by 5
External K+ Deficiency Inhibits Photosynthetic Activity Through Superoxide Anion Production in Protoplasts Isolated from the Thallus of Ulva pertusa
Goh, C., Oh, S., Jun, S.-S., & Han, T. (2010) · Journal of Plant Biology · doi:10.1007/s12374-010-9101-3 · Cited by 4
“…inhibited by the addition of 100 μM AZ to the medium under both alkaline and acidic conditions, implying that CA-mediated dehydration followed by free CO2 uptake is active at pH 6.1 and that an anion exchanger probably mediates the direct uptake of HCO3 − at pH 8.8 (Axelson et al. 2000).”
BackgroundInfluential
Estimation of Growth and Carrying Capacity of Porphyra spp. Under Aquaculture Conditions on the Southern Coast of Korea Using Dynamic Energy Budget (DEB)
Tac, D. H., Park, S.-E., & Lee, J. (2025) · Journal of Marine Science and Engineering · doi:10.3390/jmse13081586 · Cited by 2
“The model assumes the availability of dissolved CO 2 in seawater, including uptake from bicarbonate (HCO 3 − ), which is known to support photosynthetic carbon fixation in macroalgae under high-pH conditions [26].”
Erratum to: External K+ Deficiency Inhibits Photosynthetic Activity Through Superoxide Anion Production in Protoplasts Isolated from the Thallus of Ulva pertusa
Goh, C., Oh, S., Jun, S.-S., & Han, T. (2013) · Journal of Plant Biology · doi:10.1007/s12374-013-0908-6 · Cited by 2
Effects of intermittent exposure of marine pollutants on sugar kelp and periphyton
Johansson, P. (2009) · Gothenburg University Publications Electronic Archive (Gothenburg University) · Cited by 2
Species-specific responses of macrophyte production to the increasing CO2 environment with potential ecosystem implications involved in the Baltic Sea
Pajusalu, L., Albert, G., Fachon, E., Hepburn, C. D., Kotta, J., Kõivupuu, A., Paalme, T., Pritchard, D. W., Põllumäe, A., Torn, K., et al. (2023) · Journal of Applied Phycology · doi:10.1007/s10811-023-03047-3 · Cited by 1
“Since Tris buffer has been known to inhibit the productivity of some macroalgal species, the effect of Tris buffer on each experimental species was tested by measuring the O 2 evolution of individuals (Axelsson et al. 2000), and no significant effect at p < 0.05 was found.”
Influential
A simple growth model of Saccharina latissima cultivated in Scandinavia: Theoretical and practical implications
Holst, N., Boderskov, T., & Bruhn, A. (2025) · Algal Research · doi:10.1016/j.algal.2025.103971 · Cited by 1
Energy balance during active carbon uptake and at excess irradiance in three marine macrophytes
Carr, H. (2005) · KTH Publication Database DiVA (KTH Royal Institute of Technology) · Cited by 1
The effects of ocean acidification on photosynthesis, growth, and carbon and nitrogen metabolism of Macrocystis pyrifera
Subiabre, F., & Andrea, P. (2016) · Otago University Research Archive (University of Otago) · Cited by 1
External α carbonic anhydrase and solute carrier 4 (SLC4) bicarbonate transporter are required for HCO3- uptake in a freshwater angiospermPreprint
Huang, W., Han, S., Jiang, H. S., Gu, S., Wei, L., Gontero, B., & MABERLY, S. C. (2020) · doi:10.22541/au.158359580.04799453 · Cited by 1

Role of external carbonic anhydrase in light-dependent alkalization byFucus serratus L. andLaminaria saccharina (L.) Lamour. (Phaeophyta)
Haglund, K., Ramazanov, Z., Mtolera, M. S. P., & Peders�n, M. (1992) · Planta · doi:10.1007/bf01160705 · Cited by 49
Evidence for a plasmalemma-based CO2 concentrating mechanism in Laminaria saccharina
Mercado, J. M., Andría, J. R., Pérez‐Lloréns, J. L., Vergara, J. J., & Axelsson, L. (2006) · Photosynthesis Research · doi:10.1007/s11120-006-9039-y · Cited by 32
Self-citation
Bicarbonate uptake and utilization in marine macroalgae
Larsson, C. S., & Axelsson, L. (1999) · European Journal of Phycology · doi:10.1080/09670269910001736112 · Cited by 123
Self-citation
Two modes of bicarbonate utilization in the marine green macroalga Ulva lactuca
Axelsson, L., Ryberg, H., & Beer, S. (1995) · Plant Cell & Environment · doi:10.1111/j.1365-3040.1995.tb00378.x · Cited by 138
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Effects of carbon anhydrase on utilization of bicarbonate in microalgae: a case study in Lake Hongfeng
Li, H., Wu, Y., & Zhao, L. (2018) · Acta Geochimica · doi:10.1007/s11631-018-0277-4 · Cited by 13

Authors: Axelsson, L., Mercado, J., & Figueroa, F.
Affiliations: Universidad de Málaga (ES)
ORCID: Mercado, Jesús
Figueroa, Félix
Venue: European Journal of Phycology
Publisher: Informa UK Limited
Published: 2000-02
Volume: 35
Issue: 1
Pages: 53-59
ISSN: 0967-0262 (ISSN-L)
1469-4433
DOI: 10.1080/09670260010001735621
OpenAlex: W2075150504
Cited by: 107
References: 32
Citations by year: 2026: 3 · 2025: 3 · 2023: 3 · 2022: 3 · 2021: 4 · 2020: 5 · 2019: 4 · 2018: 2 · 2017: 6 · 2016: 9 · 2015: 7 · 2014: 4 · 2013: 8 · 2012: 4
FWCI: 3.96
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: European Journal of Phycology (publishedVersion)
Funders: Royal Swedish Academy of Sciences
Magnus Bergvalls Stiftelse
Topics: Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine and coastal plant biology
Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine Plankton and Biogeochemistry
Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
Keywords: Saccharina latissima, brown algae, bicarbonate utilization, carbonic anhydrase, acetazolamide, photosynthesis, CO2-concentrating mechanism, inorganic carbon uptake, seawater pH

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Utilization of HCO 3 − at high pH by the brown macroalga Laminaria saccharina

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