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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Ultraviolet radiation stimulated activity of extracellular carbonic anhydrase in the marine diatom Skeletonema costatum

Hongyan Wu A C and Kunshan Gao B
+ Author Affiliations
- Author Affiliations

A Marine Biology Institute, Shantou University, Shantou, Guangdong 515063, China.

B State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen 361005, China.

C Corresponding author. Email: wuhy@stu.edu.cn

Functional Plant Biology 36(2) 137-143 https://doi.org/10.1071/FP08172
Submitted: 18 June 2008  Accepted: 10 November 2008   Published: 5 February 2009

Abstract

Previous studies have shown that reduced levels of solar UV radiation (280–400 nm) can enhance photosynthetic carbon fixation of marine phytoplankton, but the mechanisms are not known. The supply of CO2 for photosynthesis is facilitated by extracellular (periplasmic) carbonic anhydrase (CAe) in most marine phytoplankton species. The present study showed that the CAe activity of Skeletonema costatum (Greville) Cleve was stimulated when treated with UV-A (320–395 nm) or UV-A + UV-B (295–320 nm) in addition to visible radiation. The presence of UV-A and UV-B enhanced the activity by 28% and 24%, respectively, at a low irradiance (PAR 161, UV-A 28, UV-B 0.9 W m−2) and by 21% and 19%, respectively, at a high irradiance (PAR 328, UV-A 58, UV-B 1.9 W m−2) level after exposure for 1 h. Ultraviolet radiation stimulated CAe activity contributed up to 6% of the photosynthetic carbon fixation as a result of the enhanced supply of CO2, as revealed using the CAe inhibitor (acetazolamide). As a result, there was less inhibition of photosynthetic carbon fixation compared with the apparent quantum yield of PSII. The UV radiation stimulated CAe activity coincided with the enhanced redox activity at the plasma membrane in the presence of UV-A and/or UV-B. The present study showed that UV radiation can enhance CAe activity, which plays an important role in counteracting UV inhibition of photosynthesis.

Additional keywords: CO2 acquisition, photoinhibition, photosynthesis.


Acknowledgements

This research was supported by the National Natural Science Foundation of China (No. 90411018; No. 40573059; No. 40876058), the National Basic Research Program of China (2009CB421207) and the Natural Science Foundation of Guangdong Province (No. 5300896). We are grateful to Guang Gao for his technical assistance and Brian A. Whitton for helpful comments.


References


Aizawa K, Miyachi S (1986) Carbonic anhydrase and CO2 concentrating mechanisms in microalgae and cyanobacteria. FEMS Microbiology Reviews 39, 215–233.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Badger MR, Andrews TJ, Whitney SM, Ludwig M, Yellowlees DC, Leggat W, Price GD (1998) The diversity and coevolution of Rubisco, plastid, pyrenoids and chloroplast-based CO2-concentrating mechanisms in algae. Canadian Journal of Botany 76, 1052–1071.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Barbieri E, Villafañe V, Helbling E (2002) Experimental assessment of UV effects on temperate marine phytoplankton when exposed to variable radiation regimes. Limnology and Oceanography 47, 1648–1655. open url image1

Beardall J, Heraud P, Roberts S, Shelly K, Stojkovic S (2002) Effects of UV-B radiation on inorganic carbon acquisition by the marine microalga Dunaliella tertiolecta (Chlorophyceae). Phycologia 41, 268–272. open url image1

Bischof K, Kräbs G, Wiencke C, Hanelt D (2002) Solar ultraviolet radiation affects the activity of ribulose-1,5-bisphosphate carboxylase-oxygenase and the composition of photosynthetic and xanthophyll cycle pigments in the intertidal green alga Ulva lactuca L. Planta 215, 502–509.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Bouchard JN, Campbell DA, Roy S (2005) Effects of UV-B radiation on the D1 protein repair cycle of natural phytoplankton communities from three latitudes (Canada, Brazil, and Argentina). Journal of Phycology 41, 273–286.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Bozzo GG, Colman B (2000) The induction of inorganic carbon transport and external carbonic anhydrase in Chlamydomonas reinhardtii is regulated by external CO2 concentration. Plant, Cell & Environment 23, 1137–1144.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Chen X, Gao K (2003) Effect of CO2 concentrations on the activity of photosynthetic CO2 fixation and extracelluar carbonic anhydrase in the marine diatom Skeletonema costatum. Chinese Science Bulletin 48, 2616–2620.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Chen X, Gao K (2004) Photosynthetic utilisation of inorganic carbon and its regulation in the marine diatom Skeletonema costatum. Functional Plant Biology 31, 1027–1033.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Chen X, Qiu C, Shao J (2006) Evidence for K+-dependent HCO3 − utilization in the marine diatom Phaeodactylum tricornutum. Plant Physiology 141, 731–736.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Colman B, Huertas IE, Bhatti S, Dason JS (2002) The diversity of inorganic carbon acquisition mechanism in eukaryotic microalgae. Functional Plant Biology 29, 261–270.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Dionisio ML, Tsuzuki M, Miyachi S (1989) Blue light induction of carbonic anhydrase activity in Chlamydomonas reinhardtii. Plant & Cell Physiology 30, 215–219.
CAS |
open url image1

Dionisio-Sese ML, Fukuzawa H, Miyachi S (1990) Light-induced carbonic anhydrase expression in Chlamydomonas reinhardtii. Plant Physiology 94, 1103–1110.
CAS | Crossref | PubMed |
open url image1

Franklin LA, Neale PJ (2002) Biological weighting function for the effect of UV radiation on carbon partitioning in microalgae. Journal of Phycology 38, 10.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gao K, Aruga Y, Asada K, Ishihara T, Akano T, Kiyohara M (1993) Calcification in the articulated coralline alga Corallina pilulifera, with special reference to the effect of elevated CO2 concentration. Marine Biology (Berlin) 117, 129–132.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Gao K, Wu Y, Li G, Wu H, Villafañe VE, Helbling EW (2007) Solar UV radiation drives CO2 fixation in marine phytoplankton: a double-edged sword. Plant Physiology 144, 54–59.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Genty BE, Briantais JM, Baker NR (1989) Relative quantum efficiencies of the two photosystems of leaves in photorespiratory and non-photorespiratory conditions. Plant Physiology and Biochemistry 28, 1–10. open url image1

Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annual Review of Physiology 56, 99–131.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Helbling EW, Gao K, Gonçalves RJ, Wu H, Villafañe VE (2003) Utilization of solar UV radiation by coastal phytoplankton assemblages off SE China when exposed to fast mixing. Marine Ecology Progress Series 259, 59–66.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Hobson LA, Hanson CE, Holeton C (2001) An ecological basis for extracellular carbonic anhydrase in marine unicellular algae. Journal of Phycology 37, 717–723.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochemie und Physiologie der Pflanzen 167, 191–194.
CAS |
open url image1

Korb RE, Saville PJ, Johnston AM, Raven JA (1997) Sources of inorganic carbon for photosynthesis by three species of marine diatom. Journal of Phycology 33, 433–440.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Long JC, Jenkins GI (1998) Involvement of plasma membrane redox activity and calcium homeostasis in the UV-B and UV-A/blue light induction of gene expression in Arabidopsis. The Plant Cell 10, 2077–2086.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Matsuda Y, Hara T, Colman B (2001) Regulation of the induction of bicarbonate uptake by dissolved CO2 in the marine diatom Phaeodactylum tricornutum. Plant, Cell & Environment 24, 611–620.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Nimer NA, Warren M, Merrett MJ (1998) The regulation of photosynthetic rate and activation of extracellular carbonic anhydrase under CO2-limiting conditions in the marine diatom Skeletonema costatum. Plant, Cell & Environment 21, 805–812.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Nimer NA, Brownlee C, Merrett MJ (1999a) Extrracellular carbonic anhydrase facilitates carbon dioxide availability for photosynthesis in the marine dinoflagellate Prorocentrum micans. Plant Physiology 120, 105–111.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Nimer NA, Ling MX, Brownlee C, Merritt MJ (1999b) Inorganic carbon limitation, exofacial carbonic anhydrase activity, and plasma membrane redox activity in marine phytoplankton species. Journal of Phycology 35, 1200–1205.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Raven JA (1997) Inorganic carbon acquisition by marine autotrophs. Advances in Botanical Research 27, 114–134. open url image1

Raven JA (1999) Photosynthesis in the intertidal zone: algae get an airing. Journal of Phycology 35, 1102–1105. open url image1

Raven JA , Beardall J (2003) Carbon acquisition mechanisms in algae: carbon dioxide diffusion and carbon dioxide concentrating mechanisms. In ‘Photosynthesis in algae’. (Eds AWD Larkum, SE Douglas, JA Raven) pp. 225–244. (Kluwer: Dordrecht)

Rawat M, Moroney JV (1995) The regulation of carbonic anhydrase and ribulose-1, 5-bisphosphate carboxylase/oxygenase activase by light and CO2 in Chlamydomonas reinhardtii. Plant Physiology 109, 937–944.
CAS | PubMed |
open url image1

Roberts K, Granum E, Leegood RC, Raven JA (2007) Carbon acquisition by diatoms. Photosynthesis Research 93, 79–88.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Rost B, Riebesell U, Sültemeyer D (2006) Carbon acquisition of marine phytoplankton: effect of photoperiod length. Limnology and Oceanography 51, 12–20.
CAS |
open url image1

Rubinstein B, Luster DG (1993) Plasma membrane redox activity: components and role in plant processes. Annual Review of Plant Physiology and Plant Molecular Biology 44, 131–155.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Sobrino C, Montero O, Lubian L (2004) UV-B radiation increases cell permeability and damages nitrogen incorporation mechanisms in Nannochloropsis gaditana. Aquatic Sciences 66, 421–429.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sobrino C, Ward ML, Neale P (2008) Acclimation to elevated carbon dioxide and ultraviolet radiation in the diatom Thalassiosira pseudonana: effects on growth, photosynthesis, and spectral sensitivity of photoinhibition. Limnology and Oceanography 53, 494–505.
CAS |
open url image1

Stumm W , Morgan JJ (1995) Chemical equilibria and rates in natural waters. In ‘Environmental science and technology, aquatic chemistry’. (Eds JL Schnoor, A Zehnder) pp. 148–201 (John Wiley & Sons: New York)

Sültemeyer D (1998) Carbonic anhydrase in eukaryotic algae: characterization, regulation, and possible function during photosynthesis. Canadian Journal of Botany 76, 962–972.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sun B, Liang S, Wang C, Wang X, Wang X, Li Y (2008) Role of irradiance on the seasonality of Skeletonema costatum Cleve blooms in the coastal area in east China sea. Environmental Sciences (Tokyo) [with English abstract] 29, 1849–1854. open url image1

Wilbur KM, Anderson NG (1948) Electrometric and colorimetric determination of carbonic anhydrase. Journal of Biological Chemistry 176, 147–154.
CAS | PubMed |
open url image1