Skip to main content
SpringerLink
Log in

Effect of elevated carbon dioxide and nitric oxide on the physiological responses of two green algae, Asterarcys quadricellulare and Chlorella sorokiniana

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Algae have the potential to capture carbon dioxide (CO2) and nitric oxide (NO) from flue gases. However, the effects of high concentrations of these gases on the photophysiology of algae are poorly understood. To that end, we used the techniques of chlorophyll fluorescence to study the effect of industrially relevant levels of CO2 and NO on the photophysiology of two green microalgae, Asterarcys quadricellulare and Chlorella sorokiniana, that are tolerant to these gases. Measurements of maximum quantum yield (Fv/Fm) and maximum relative electron transport rate (rETRmax) show an enhanced performance of photosystem II (PSII) under high CO2 levels. In C. sorokiniana, high CO2 stimulated non-photochemical quenching (NPQ), while the opposite effect was observed in A. quadricellulare. Light-saturated photosynthetic rates (Pmax) of both species were highest at 10% CO2. Further, the tested levels of NO did not show adverse effect on the performance of PSII. OJIP chlorophyll fluorescence transients suggest that in C. sorokiniana, the energetic communication between PSII units declined at 15% CO2. However, in A. quadricellulare, this decline was visible even at 10% CO2 with complete inhibition of cell growth at 15% v/v. Overall, our results suggest that although photosynthesis was regulated differently in the two microalga, both species exhibited enhanced PSII performance under reasonably high levels of CO2 and NO. Thus, the two species are potential candidates for bio-fixation of CO2 and NO from flue gases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30:258–270

    Article  CAS  PubMed  Google Scholar 

  • Antal T, Rubin A (2008) In vivo analysis of chlorophyll a fluorescence induction. Photosynth Res 96:217–226

    Article  CAS  PubMed  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  CAS  PubMed  Google Scholar 

  • Basu S, Roy AS, Mohanty K, Ghoshal AK (2013) Enhanced CO2 sequestration by a novel microalga: Scenedesmus obliquus SA1 isolated from bio-diversity hotspot region of Assam, India. Bioresour Technol 143:369–377

    Article  CAS  PubMed  Google Scholar 

  • Bernacchi CJ, Morgan PB, Ort DR, Long SP (2005) The growth of soybean under free air [CO2] enrichment (FACE) stimulates photosynthesis while decreasing in vivo Rubisco capacity. Planta 220:434–446

    Article  CAS  PubMed  Google Scholar 

  • Bhola VK, Swalaha FM, Nasr M, Kumari S, Bux F (2016) Physiological responses of carbon-sequestering microalgae to elevated carbon regimes. Eur J Phycol 51:401–412

    Article  CAS  Google Scholar 

  • Black MT, Brearley TH, Horton P (1986) Heterogeneity in chloroplast photosystem II. Photosynth Res 8:193–207

    Article  CAS  PubMed  Google Scholar 

  • Chiu SY, Kao CY, Chen CH, Kuan TC, Ong SC, Lin CS (2008) Reduction of CO2 by a high-density culture of Chlorella sp. in a semicontinuous photobioreactor. Bioresour Technol 99:3389–3396

    Article  CAS  PubMed  Google Scholar 

  • Chiu SY, Kao CY, Tsai MT, Ong SC, Chen CH, Lin CS (2009) Lipid accumulation and CO2 utilization of Nannochloropsis oculata in response to CO2 aeration. Bioresour Technol 100:833–838

    Article  CAS  PubMed  Google Scholar 

  • Chiu SY, Kao CY, Huang TT, Lin CJ, Ong SC, Chen CD, Chang JS, Lin CS (2011) Microalgal biomass production and on-site bioremediation of carbon dioxide, nitrogen oxide and sulfur dioxide from flue gas using Chlorella sp. cultures. Bioresour Technol 102:9135–9142

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove J, Borowitzka MA (2010) Chlorophyll fluorescence terminology: an introduction. In: Suggett DJ, Prášil O, Borowitzka MA (eds) Chlorophyll a Fluorescence in Aquatic Sciences: Methods and Applications. Springer, Dordrecht, pp 1–17

    Google Scholar 

  • Dao LHT, Beardall J (2016a) Effects of lead on two green microalgae Chlorella and Scenedesmus: photosystem II activity and heterogeneity. Algal Res 16:150–159

    Article  Google Scholar 

  • Dao LHT, Beardall J (2016b) Effects of lead on growth, photosynthetic characteristics and production of reactive oxygen species of two freshwater green algae. Chemosphere 147:420–429

    Article  CAS  PubMed  Google Scholar 

  • De Marchin T, Ghysels B, Nicolay S, Franck F (2014) Analysis of PSII antenna size heterogeneity of Chlamydomonas reinhardtii during state transitions. BBA-Bioenergetics 1837:121–130

    Article  CAS  PubMed  Google Scholar 

  • Eilers PHC, Peeters JCH (1988) A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol Model 42:199–215

    Article  Google Scholar 

  • Falk S, Palmqvist K (1992) Photosynthetic light utilization efficiency, photosystem II heterogeneity, and fluorescence quenching in Chlamydomonas reinhardtii during the induction of the CO2-concentrating mechanism. Plant Physiol 100:685–691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Guenther JE, Melis A (1990) The physiological significance of photosystem II heterogeneity in chloroplasts. Photosynth Res 23:105–109

    Article  CAS  PubMed  Google Scholar 

  • Henley WJ (1993) Measurement and interpretatiom of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. J Phycol 29:729–739

    Article  Google Scholar 

  • Henley WJ (1995) On the measurement and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. J Phycol 31:674

    Article  Google Scholar 

  • Ihnken S, Kromkamp JC, Beardall J (2011) Photoacclimation in Dunaliella tertiolecta reveals a unique NPQ pattern upon exposure to irradiance. Photosynth Res 110:123–137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iwasaki I, Kurano N, Miyachi S (1996) Effects of high-CO2 stress on photosystem II in a green alga, Chlorococcum littorale, which has a tolerance to high CO2. J Photochem Photobiol B Biol 36:327–332

    Article  CAS  Google Scholar 

  • Jianrong XIA, Qiran T (2009) Early stage toxicity of excess copper to photosystem II of Chlorella pyrenoidosa–OJIP chlorophyll a fluorescence analysis. J Environ Sci 21:1569–1574

    Article  CAS  Google Scholar 

  • Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI, Brestic M, Bussotti F, Calatayud A, Dąbrowski P, Elsheery NI, Ferroni L, Guidi L, Hogewoning SW, Jajoo A, Misra AN, Nebauer SG, Pancaldi S, Penella C, Poli D, Pollastrini M, Romanowska-Duda ZB, Rutkowska B, Serôdio J, Suresh K, Szulc W, Tambussi E, Yanniccari M, Zivcak M (2014) Frequently asked questions about in vivo chlorophyll fluorescence: Practical issues. Photosynth Res 122:121–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamalanathan M, Pierangelini M, Shearman LA, Gleadow R, Beardall J (2016) Impacts of nitrogen and phosphorus starvation on the physiology of Chlamydomonas reinhardtii. J Appl Phycol 28:1509–1520

    Article  CAS  Google Scholar 

  • Kyle DJ, Haworth P, Arntzen CJ (1982) Thylakoid membrane protein phosphorylation leads to a decrease in connectivity between photosystem II reaction centers. Biochim Biophys Acta Bioenerg 680:336–342

    Article  CAS  Google Scholar 

  • Lavergne J, Trissl HW (1995) Theory of fluorescence induction in photosystem II: derivation of analytical expressions in a model including exciton-radical-pair equilibrium and restricted energy transfer between photosynthetic units. Biophys J 68:2474–2492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li T, Tao Q, Di Z, Lu F, Yang X (2015) Effect of elevated CO2 concentration on photosynthetic characteristics of hyperaccumulator Sedum alfredii under cadmium stress. J Integr Plant Biol 57:653–660

    Article  CAS  PubMed  Google Scholar 

  • Li T, Kirchhoff H, Gargouri M, Feng J, Cousins AB, Pienkos PT, Gang DR, Chen S (2016) Assessment of photosynthesis regulation in mixotrophically cultured microalga Chlorella sorokiniana. Algal Res 19:30–38

    Article  Google Scholar 

  • Ma S, Li D, Yu Y, Li D, Yadav RS, Feng Y (2019) Application of a microalga, Scenedesmus obliquus PF3, for the biological removal of nitric oxide (NO) and carbon dioxide. Environ Pollut 252:344–351

    Article  CAS  PubMed  Google Scholar 

  • Makino A, Mae T (1999) Photosynthesis and plant growth at elevated levels of CO2. Plant Cell Physiol 40:999–1006

    Article  CAS  Google Scholar 

  • Markou G, Depraetere O, Muylaert K (2016) Effect of ammonia on the photosynthetic activity of Arthrospira and Chlorella: a study on chlorophyll fluorescence and electron transport. Algal Res 16:449–457

    Article  Google Scholar 

  • Markou G, Dao LHT, Muylaert K, Beardall J (2017) Influence of different degrees of N limitation on photosystem II performance and heterogeneity of Chlorella vulgaris. Algal Res 26:84–92

    Article  Google Scholar 

  • Masojídek J, Vonshak A, Torzillo G (2010) Chlorophyll a fluorescence applications in microalgal mass cultures. In: Suggett DJ, Prášil O, Borowitzka MA (eds) Chlorophyll a Fluorescence in Aquatic Sciences: Methods and Applications. Springer, Dordrecht, pp 277–292

    Chapter  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • Melis A, Neidhardt J, Benemann JR (1998) Dunaliella salina (Chlorophyta) with small chlorophyll antenna sizes exhibit higher photosynthetic productivities and photon use efficiencies than normally pigmented cells. J Appl Phycol 10:515–525

    Article  Google Scholar 

  • Mende D (1980) Evidence for a cyclic PS-II-electron transport in vivo. Plant Sci Lett 17:215–220

    Article  CAS  Google Scholar 

  • Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

    Article  PubMed  PubMed Central  Google Scholar 

  • Nagase H, Yoshihara KI, Eguchi K, Yokota Y, Matsui R, Hirata K, Miyamoto K (1997) Characteristics of biological NOx removal from flue gas in a Dunaliella tertiolecta culture system. J Ferment Bioeng 83:461–465

    Article  CAS  Google Scholar 

  • Nagase H, Yoshihara K, Eguchi K, Okamoto Y, Murasaki S, Yamashita R, Hirata K, Miyamoto K (2001) Uptake pathway and continuous removal of nitric oxide from flue gas using microalgae. Biochem Eng J 7:241–246

    Article  CAS  Google Scholar 

  • Nedbal L, Trtílek M, Kaftan D (1999) Flash fluorescence induction: a novel method to study regulation of photosystem II. J Photochem Photobiol B Biol 48:154–157

    Article  CAS  Google Scholar 

  • Pierangelini M, Stojkovic S, Orr PT, Beardall J (2014a) Photosynthetic characteristics of two Cylindrospermopsis raciborskii strains differing in their toxicity. J Phycol 50:292–302

    Article  CAS  PubMed  Google Scholar 

  • Pierangelini M, Stojkovic S, Orr PT, Beardall J (2014b) Elevated CO2 causes changes in the photosynthetic apparatus of a toxic cyanobacterium, Cylindrospermopsis raciborskii. J Plant Physiol 171:1091–1098

    Article  CAS  PubMed  Google Scholar 

  • Qiu B, Gao K (2002) Effects of CO2 enrichment on the bloom-forming cyanobacterium Microcystis Aeruginosa (Cyanophyceae): Physiological responses and relationships with the availability of dissolved inorganic carbon. J Phycol 38:721–729

    Article  CAS  Google Scholar 

  • Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat Bot 82:222–237

    Article  CAS  Google Scholar 

  • Raven JA, Beardall J, Giordano M (2014) Energy costs of carbon dioxide concentrating mechanisms in aquatic organisms. Photosynth Res 121:111–124

    Article  CAS  PubMed  Google Scholar 

  • Ruban AV, Johnson MP, Duffy CDP (2011) Natural light harvesting: principles and environmental trends. Energy Environ Sci 4:1643–1650

    Article  CAS  Google Scholar 

  • Schmitz P, Maldonado-Rodriguez R (2001) Evaluation of the nodulated status of Vigna unguiculata probed by the JIP test based on the chlorophyll a fluorescence rise. In: 12th International Photosynthesis Congress. Brisbane, Australia,

  • Sebök S, Herppich WB, Hanelt D (2017) Red alga Palmaria palmata—growth rate and photosynthetic performance under elevated CO2 treatment. J Appl Phycol 29:381–393

    Article  CAS  Google Scholar 

  • Seth JR, Wangikar PP (2015) Challenges and opportunities for microalgae-mediated CO2 capture and biorefinery. Biotechnol Bioeng 112:1281–1296

    Article  CAS  PubMed  Google Scholar 

  • Spalding MH, Critchley C, Govindjee, Orgren WLO (1984) Influence of carbon dioxide concentration during growth on fluorescence induction characteristics of the green alga Chlamydomonas reinhardii. Photosynth Res 5:169–176

    Article  CAS  PubMed  Google Scholar 

  • Stirbet A, Govindjee SBJ, Strasser RJ (1998) Chlorophyll a fluorescence induction in higher plants: modelling and numerical simulation. J Theor Biol 193:131–151

    Article  CAS  Google Scholar 

  • Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plant and cyanobacteria. Photochem Photobiol 61:32–42

    Article  CAS  Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgio GC, Govindjee (eds) Chlorophyll a Fluorescence: A Signature of Photosynthesis. Springer, Dordrecht, pp 321–362

    Chapter  Google Scholar 

  • Tchernov D, Hassidim M, Vardi A, Luz B, Sukenik A, Reinhold L, Kaplan A (1998) Photosynthesizing marine microorganisms can constitute a source of CO2 rather than a sink. Can J Bot 76:949–953

    Google Scholar 

  • Varshney P, Mikulic P, Vonshak A, Beardall J, Wangikar PP (2015) Extremophilic micro-algae and their potential contribution in biotechnology. Bioresour Technol 184:363–372

    Article  CAS  PubMed  Google Scholar 

  • Varshney P, Sohoni S, Wangikar PP, Beardall J (2016) Effect of high CO2 concentrations on the growth and macromolecular composition of a heat- and high-light-tolerant microalga. J Appl Phycol 28:2631–2640

    Article  CAS  Google Scholar 

  • Varshney P, Beardall J, Bhattacharya S, Wangikar PP (2018) Isolation and biochemical characterisation of two thermophilic green algal species- Asterarcys quadricellulare and Chlorella sorokiniana, which are tolerant to high levels of carbon dioxide and nitric oxide. Algal Res 30:28–37

    Article  Google Scholar 

  • Vincent WF, Roy S (1993) Solar ultraviolet-B radiation and aquatic primary production: Damage, protection, and recovery. Environ Rev 1:1–12

    Article  CAS  Google Scholar 

  • Vinet L, Zhedanov A (2011) A ‘missing’ family of classical orthogonal polynomials. J Phys A Math Theor 44:085201

    Article  Google Scholar 

  • Yang Y, Gao K (2003) Effects of CO2 concentrations on the freshwater microalgae, Chlamydomonas reinhardtii, Chlorella pyrenoidosa and Scenedesmus obliquus (Chlorophyta). J Appl Phycol 15:379–389

    Article  CAS  Google Scholar 

  • Yoshihara K-I, Hiroyasu N, Eguchi K, Hirata K (1996) Biological elimination of nitric oxide and carbon dioxide from flue gas by marine microalga NOA-13 cultivated in a long tubular photobioreactor. J Ferment Bioeng 82:351–354

    Article  CAS  Google Scholar 

  • Zhang D, Pan X, Mu G, Wang J (2010a) Toxic effects of antimony on photosystem II of Synechocystis sp. as probed by in vivo chlorophyll fluorescence. J Appl Phycol 22:479–488

    Article  CAS  Google Scholar 

  • Zhang T, Gong H, Wen X, Lu C (2010b) Salt stress induces a decrease in excitation energy transfer from phycobilisomes to photosystem II but an increase to photosystem I in the cyanobacterium Spirulina platensis. J Plant Physiol 167:951–958

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Pei H, Hu W, Qi F, Han L, Song M, Han F (2015) Biomass and lipid accumulation of three new screened microalgae with high concentration of carbon dioxide and nitric oxide. Environ Technol 36:2278–2284

    Article  CAS  PubMed  Google Scholar 

  • Zhao B, Wang J, Gong H, Wen X, Ren H, Lu C (2008) Effects of heat stress on PSII photochemistry in a cyanobacterium Spirulina platensis. Plant Sci 175:556–564

    Article  CAS  Google Scholar 

  • Zhao B, Su Y, Zhang Y, Cui G (2015) Carbon dioxide fixation and biomass production from combustion flue gas using energy microalgae. Energy 89:347–357

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the JSW Foundation, India, Wadhwani Research Centre for Bioengineering, IIT Bombay, India and the Department of Biotechnology, Ministry of Science and Technology, Government of India (Grant No: BT/EB/PAN IIT/2012).

Author information

Authors and Affiliations

  1. IITB-Monash Research Academy, Indian Institute of Technology Bombay, Powai, Mumbai, Maharashtra, India

    Prachi Varshney

  2. Department of Chemical Engineering, Indian Institute of Technology Bombay, Powai, Mumbai, Maharashtra, India

    Prachi Varshney & Pramod P. Wangikar

  3. School of Biological Sciences, Monash University, Clayton, Melbourne, Victoria, Australia

    Prachi Varshney & John Beardall

  4. Department of Chemical Engineering, Monash University, Clayton, Melbourne, Victoria, Australia

    Prachi Varshney & Sankar Bhattacharya

  5. DBT-Pan IIT Centre for Bioenergy, Indian Institute of Technology Bombay, Powai, Mumbai, Maharashtra, India

    Pramod P. Wangikar

  6. Wadhwani Research Centre for Bioengineering, Indian Institute of Technology Bombay, Powai, Mumbai, Maharashtra, India

    Pramod P. Wangikar

Authors
  1. Prachi Varshney
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John Beardall
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sankar Bhattacharya
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pramod P. Wangikar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pramod P. Wangikar.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 166 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Varshney, P., Beardall, J., Bhattacharya, S. et al. Effect of elevated carbon dioxide and nitric oxide on the physiological responses of two green algae, Asterarcys quadricellulare and Chlorella sorokiniana. J Appl Phycol 32, 189–204 (2020). https://doi.org/10.1007/s10811-019-01950-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-019-01950-2

Keywords

Search

Navigation