Effects of carbon anhydrase on utilization of bicarbonate in microalgae: a case study in Lake Hongfeng

Haitao Li1,2, Yanyou Wu2, Lihua Zhao2
1School of Karst Science, Guizhou Normal University / State Engineering Technology Institute for Karst Desertfication Control, Guiyang, China
2State Key Laboratory of Environmental Geochemistry, Institute of Geochemistry, Chinese Academy of Sciences, Guiyang, China

Tóm tắt

A bidirectional labeling method was established to distinguish the proportions of HCO3− and CO2 utilization pathways of microalgae in Lake Hongfeng. The method was based on microalgae cultured in a medium by adding equal concentrations of NaH13CO3 with different δ13C values simultaneously. The inorganic carbon sources were quantified according to the stable carbon isotope composition in the treated microalgae. The effects of extracellular carbonic anhydrase (CAex) on the HCO3− and CO2 utilization pathways were distinguished using acetazolamide, a potent membrane-impermeable carbonic anhydrase inhibitor. The results show utilization of the added HCO3− was only 8% of the total carbon sources in karst lake. The proportion of the HCO3− utilization pathway was 52% of total inorganic carbon assimilation. Therefore, in the natural water of the karst area, the microalgae used less bicarbonate that preexisted in the aqueous medium than CO2 derived from the atmosphere. CAex increased the utilization of inorganic carbon from the atmosphere. The microalgae with CAex had greater carbon sequestration capacity in this karst area.

Từ khóa


Tài liệu tham khảo

Axelsson L, Ryberg H, Beer S (1995) Two modes of bicarbonate utilization in the marine green macroalga ulva lactuca. Plant Cell Environ 18:439–445

Bade DL, Pace ML, Cole JJ, Carpenter SR (2006) Can algal photosynthetic inorganic carbon isotope fractionation be predicted in lakes using existing models? Aquat Sci 68:142–153

Badger MR, Price GD (1994) The role of carbonic anhydrase in photosynthesis. Annu Rev Plant Biol 45:369–392

Chen Z, Cheng HM, Chen XW (2009) Effect of Cl− on photosynthetic bicarbonate uptake in two cyanobacteria Microcystis aeruginosa and Synechocystis PCC6803. Chin Sci Bull 54:1197–1203

Colman B, Huertas IE, Bhatti S, Dason JS (2002) The diversity of inorganic carbon acquisition mechanisms in eukaryotic microalgae. Funct Plant Biol 29:261–270

Elzenga JTM, Prins HBA, Stefels J (2000) The role of extracellular carbonic anhydrase activity in inorganic carbon utilization of phaeocystis globosa (prymnesiophyceae): A comparison with other marine algae using the isotopic disequilibrium technique. Limnol Oceanogr 45:372–380

Fry B, Sherr EB (1984) δ13C measurements as indicators of carbon flow on marine and freshwater ecosystems. Contrib Mar Sci 27:13–47

Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131

Marlier JF, O’Leary MH (1984) Carbon kinetic isotope effects on the hydration of carbon dioxide and the dehydration of bicarbonate ion. J Am Chem Soc 106:5054–5057

Moazami-Goudarzi M, Colman B (2011) Inorganic carbon acquisition in two green marine stichococcus species. Plant Cell Environ 34:1465–1472

Mondal M, Khanra S, Tiwari ON, Gayen K, Halder GN (2016) Role of carbonic anhydrase on the way to biological carbon capture through microalgae-a mini review. Environ Progress Sustain Energy 35(6):1605–1615

Mook WG, Bommerson JC, Staverman WH (1974) Carbon isotope fractionation between dissolved bicarbonate and gaseous carbon dioxide. Earth Planet Sci Lett 22(2):169–1769

Moroney JV, Husic HD, Tolbert N (1985) Effect of carbonic anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. Plant Physiol 79:177–183

Moulin P, Andría JR, Axelsson L, Mercado JM (2011) Different mechanisms of inorganic carbon acquisition in red macroalgae (Rhodophyta) revealed by the use of TRIS buffer. Aquat Bot 95:31–38

Riebesell U, Wolf-Gladrow DA, Smetacek V (1993) Carbon dioxide limitation of marine phytoplankton growth rates. Nature 361:249–251

Sedmak JJ, Grossberg SE (1977) A rapid, sensitive, and versatile assay for protein using Coomassie brilliant blue G250. Anal Biochem 79:544–552

Smith-Harding TJ, Beardall J, Mitchell JG (2017) The role of external carbonic anhydrase in photosynthesis during growth of the marine diatom Chaetoceros muelleri. J Phycol 53(6):1159–1170

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

Talling JF (1976) The depletion of carbon dioxide from lake water by phytoplankton. J Ecol 64(1):79–121

White DA, Pagarette A, Rooks P, Ali ST (2013) The effect of sodium bicarbonate supplementation on growth and biochemical composition of marine microalgae cultures. J Appl Phycol 25(1):153–165

Williams TG, Turpin DH (1987) The role of external carbonic anhydrase in inorganic carbon acquisition by chlamydomonas reinhardii at alkaline pH. Plant Physiol 83:92–96

Wu YY, Li PP, Wang BL, Liu CQ, He M, Chen CH (2008) Composition and activity of external carbonic anhydrase of microalgae from karst lakes in China. Phycol Res 56:76–82

Wu YY, Xu Y, Li HT, Xing DK (2012) Effect of acetazolamide on stable carbon isotope fractionation in chlamydomonas reinhardtii and chlorella vulgaris. Chin Sci Bull 57:786–789

Xie TX, Wu YY (2017) The biokarst system and its carbon sinks in response to pH changes: a simulation experiment with microalgae. Geochem Geophys Geosyst 18:827–843