The contribution of biophysical and biochemical CO2 concentration mechanisms to the carbon fixation of the green macroalga Ulva prolifera

Xiaohua Zhang , Guang Gao , Zhengquan Gao , Kunshan Gao , Dongyan Liu

Marine Life Science & Technology ›› 2025, Vol. 7 ›› Issue (3) : 537 -548.

PDF
Marine Life Science & Technology ›› 2025, Vol. 7 ›› Issue (3) : 537 -548. DOI: 10.1007/s42995-024-00265-7
Research Paper
research-article

The contribution of biophysical and biochemical CO2 concentration mechanisms to the carbon fixation of the green macroalga Ulva prolifera

Author information +
History +
PDF

Abstract

CO2 concentration mechanisms (CCMs) are important in maintaining the high efficiency of photosynthesis of marine algae. Aquatic photoautotrophs have two types of CCMs: biophysical CCMs, based on the conversion of inorganic carbon, and biochemical CCMs, based on the formation of C4 acid intermediates. However, the contribution of biophysical and biochemical CCMs to algal carbon fixation remains unclear. Here, we used ethoxyzolamide (EZ) inhibitors of carbonic anhydrase and 3-mercaptopicolinic acid (MPA) inhibitors for phosphoenolpyruvate carboxykinase to examine the importance of biophysical and biochemical CCMs in photosynthesis of the green macroalga Ulva prolifera. The culture experiments showed that the carbon fixation of the species declined when EZ inhibited the biophysical CCM, while the increase in cyclic electron flow around the photosystem I indicated a more active biochemical CCM, contributing to ~ 50% of total carbon fixation. The biophysical CCM was also reinforced when MPA inhibited the biochemical CCM. In a comparison, the biophysical CCM can compensate for almost 100% of total carbon fixation. The results indicate that biophysical CCMs dominate the process of carbon fixation of U. prolifera while biochemical CCM plays a supporting role. Our results provide evidence of a complementary coordination mechanism between the biophysical and biochemical CCMs that promotes the efficiency of photosynthesis of U. prolifera, an efficient mechanism to boost the alga’s bloom.

Special Topic: Ecology & Environmental Biology.

The online version contains supplementary material available at https://doi.org/10.1007/s42995-024-00265-7.

Keywords

CO2 concentration mechanism / Photosynthesis / Carbon fixation / Carbonic anhydrase / C4 metabolism

Cite this article

Download citation ▾
Xiaohua Zhang, Guang Gao, Zhengquan Gao, Kunshan Gao, Dongyan Liu. The contribution of biophysical and biochemical CO2 concentration mechanisms to the carbon fixation of the green macroalga Ulva prolifera. Marine Life Science & Technology, 2025, 7(3): 537-548 DOI:10.1007/s42995-024-00265-7

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

BeardallJ, RavenJAWangQ. Acquisition of inorganic carbon by microalgae and cyanobacteria. Microbial photosynthesis, 2020, Singapore. Springer. 151168.

[2]

BeerS. Photosynthetic traits of the ubiquitous and prolific macroalga Ulva (Chlorophyta): a review. Eur J Phycol, 2022, 58: 390-398.

[3]

BeerS, IsraelA, DrechslerZ, CohenY. Photosynthesis in Ulva fasciata: V. Evidence for an inorganic carbon concentrating system, and ribulose-1,5-bisphosphate carboxylase/oxygenase CO2 kinetics. Plant Physiol, 1990, 94: 1542-1546.

[4]

BergesJA, FranklinDJ, HarrisonPJ. Evolution of an artificial seawater medium: improvements in enriched seawater, artificial water over the last two decades. J Phycol, 2001, 37: 1138-1145.

[5]

BjörkM, HaglundK, RamazanovZ, Garcia-ReinaG, PedersénM. Inorganic-carbon assimilation in the green seaweed Ulva rigida C.Ag. (Chlorophyta). Planta, 1992, 187: 152-156.

[6]

BowesGW. Carbonic anhydrase in marine algae. Plant Physiol, 1969, 44: 726-732.

[7]

BurlacotA, DaoO, AuroyP, CuinéS, Li-BeissonY, PeltierG. Alternative photosynthesis pathways drive the algal CO2-concentrating mechanism. Nature, 2022, 605: 366-371.

[8]

ChenR, CaiC, JiangT, HuangY, HeP. Growth and metagenomics analysis of Ulva prolifera after antibiotic treatment. Int J Agric Biol, 2019, 21: 1031-1035

[9]

ClementR, DimnetL, MaberlySC, GonteroB. The nature of the CO2-concentrating mechanisms in a marine diatom, Thalassiosira pseudonana. New Phytol, 2016, 209: 1417-1427.

[10]

CuiJ, ZhangJ, HuoY, ZhouL, WuQ, ChenL, YuK, HeP. Adaptability of free—floating green tide algae in the Yellow Sea to variable temperature and light intensity. Mar Pollut Bull, 2015, 101: 660-666.

[11]

DrechslerZ, BeerS. Utilization of inorganic carbon by Ulva lactuca. Plant Physiol, 1991, 97: 1439-1444.

[12]

GaoK. Research techniques and methods in characterizing photosynthetic carbon fixation by algae. Mar Sci, 1999, 23: 37-41

[13]

GeeCW, NiyogiKK. The carbonic anhydrase CAH1 is an essential component of the carbon-concentrating mechanism in Nannochloropsis oceanica. Proc Natl Acad Sci USA, 2017, 114: 4537-4542.

[14]

GuK, LiuY, JiangT, CaiC, ZhaoH, LiuX, HeP. Molecular response of Ulva prolifera to short-term high light stress revealed by a multi-omics approach. Biology (Basel), 2022, 111563

[15]

Haimovich-DayanM, GarfinkelN, EweD, MarcusY, GruberA, WagnerH, KrothPG, KaplanA. The role of C4 metabolism in the marine diatom Phaeodactylum tricornutum. New Phytol, 2013, 197: 177-185.

[16]

HamaT, MiyazakiT, OgawaY, IwakumaT, TakahashiM, OtsukiA, IchimuraS. Measurement of photosynthetic production of a marine phytoplankton population using a stable 13C isotope. Mar Biol, 1983, 73: 31-36.

[17]

HiraokaM, KinoshitaY, HigaM, TsubakiS, MonotillaAP, OndaA, DanA. Fourfold daily growth rate in multicellular marine alga Ulva meridionalis. Sci Rep, 2020, 1012606.

[18]

HuangW, YangY, HuH, ZhangS, CaoK. Evidence for the role of cyclic electron flow in photoprotection for oxygen-evolving complex. J Plant Physiol, 2016, 194: 283-298.

[19]

JohnstonAM, RavenJA, BeardallJ, LeegoodRC. Photosynthesis in a marine diatom. Nature, 2001, 412: 40-41.

[20]

KaplanA. The role of C4 metabolism in the marine diatom Phaeodactylum tricornutum. New Phytol, 2013, 197: 177-185.

[21]

KochM, BowesG, RossC, ZhangX. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Chang Biol, 2013, 19: 103-132.

[22]

KonoM, NoguchiK, TerashimaI. Roles of the cyclic electron flow around PSI (CEF-PSI) and O2-dependent alternative pathways in regulation of the photosynthetic electron flow in short-term fluctuating light in Arabidopsis thaliana. Plant Cell Physiol, 2014, 55: 990-1004.

[23]

LiH, ZhangY, HanX, ShiX, RivkinRB, LegendreL. Growth responses of Ulva prolifera to inorganic and organic nutrients: implications for macroalgal blooms in the southern Yellow Sea. China Sci Rep, 2016, 626498.

[24]

LiuD, KeesingJK, HeP, WangZ, ShiY, WangY. The world's largest macroalgal bloom in the Yellow Sea, China: formation and implications. Estuar Coast Shelf Sci, 2013, 129: 2-10.

[25]

LiuD, MaQ, ValielaI, AndersonDM, KeesingJK, GaoK, ZhenY, SunX, WangY. Role of C4 carbon fixation in Ulva prolifera, the macroalga responsible for the world’s largest green tides. Commun Biol, 2020, 3494.

[26]

MaberlySC, GonteroB. Ecological imperatives for aquatic CO2-concentrating mechanisms. J Exp Bot, 2017, 68: 3797-3814.

[27]

MatsudaY, HopkinsonBM, NakajimaK, DupontCL, TsujiY. Mechanisms of carbon dioxide acquisition and CO2 sensing in marine diatoms: a gateway to carbon metabolism. Philos Trans R Soc Lond B Biol Sci, 2017, 37220160403.

[28]

McGinnPJ, MorelFM. Expression and inhibition of the carboxylating and decarboxylating enzymes in the photosynthetic C4 pathway of marine diatoms. Plant Physiol, 2008, 146: 300-309.

[29]

MoroneyJV, MaY, FreyWD, FusilierKA, PhamTT, SimmsTA, DiMarioRJ, YangJ, MukherjeeB. The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. Photosynth Res, 2011, 109: 133-149.

[30]

RavenJA, JohnB, PatriciaSB. The possible evolution and future of CO2-concentrating mechanisms. J Exp Bot, 2017, 68: 3701-3716.

[31]

ReinfelderJR. Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Ann Rev Mar Sci, 2011, 3: 291-315.

[32]

ReinfelderJR, KraepielAM, MorelFM. Unicellular C4 photosynthesis in a marine diatom. Nature, 2000, 407: 996-999.

[33]

ReiskindJB, BowesG. The role of phosphoenolpyruvate carboxykinase in a marine macroalga with C4-like photosynthetic characteristics. Proc Natl Acad Sci USA, 1991, 88: 2883-2887.

[34]

RobertsK, GranumE, LeegoodRC, RavenJA. C3 and C4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control. Plant Physiol, 2007, 145: 230-235.

[35]

SalvucciME, BowesG. Two photosynthetic mechanisms mediating the low photorespiratory state in submersed aquatic angiosperms. Plant Physiol, 1983, 73: 488-496.

[36]

ValielaI, LiuD, LloretJ, ChenowethK, HanacekD. Stable isotopic evidence of nitrogen sources and C4 metabolism driving the worldʼs largest macroalgal green tides in the Yellow Sea. Sci Rep, 2018, 817437.

[37]

WangY, StessmanDJ, SpaldingMH. The CO2 concentrating mechanism and photosynthetic carbon assimilation in limiting CO2: how Chlamydomonas works against the gradient. Plant J, 2015, 82: 429-448.

[38]

WangY, LiuF, WangM, MoejesFW, BiY. Characterization and transcriptional analysis of one carbonic anhydrase gene in the green-tide-forming alga Ulva prolifera (Ulvophyceae, Chlorophyta). Photosynth Res, 2020, 68: 90-97

[39]

WangY, LiuF, LiuM, ShiS, BiY, ChenN. Molecular cloning and transcriptional regulation of two γ-carbonic anhydrase genes in the green macroalga Ulva prolifera. Genetica, 2021, 149: 63-72.

[40]

WilburKM, AndersonNG. Electronic and colorimetric determination of carbonic anhydrase. J Biol Chem, 1948, 176: 147-154.

[41]

XuJ, FanX, ZhangX, XuD, MouS, CaoS, ZhengZ, MiaoJ, YeN. Evidence of coexistence of C3 and C4 photosynthetic pathways in a green-tide-forming alga, Ulva Prolifera. Plos ONE, 2012, 7e37438.

[42]

ZhangY, HeP, LiH, LiG, LiuJ, JiaoF, ZhangJ, HuoY, ShiX, SuR, YeN, LiuD, YuR, WangZ, ZhouM, JiaoN. Ulva prolifera green-tide outbreaks and their environmental impact in the Yellow Sea, China. Natl Sci Rev, 2019, 6: 825-838.

[43]

ZhaoH, LiuX, JiangT, CaiC, GuK, LiuY, HeP. Activated abscisic acid pathway and C4 pathway, inhibited cell cycle progression, responses of Ulva prolifera to short term high temperature elucidated by multi-omics. Mar Environ Res, 2023, 183105796.

[44]

Zuñiga-RiosD, Vásquez-ElizondoRM, CaamalE, RobledoD. Photosynthetic responses of Halimeda scabra (Chlorophyta, Bryopsidales) to interactive effects of temperature, pH, and nutrients and its carbon pathways. PeerJ, 2021, 9e10958.

RIGHTS & PERMISSIONS

The Author(s)

AI Summary AI Mindmap
PDF

197

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/