Advertisement

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

  • Prachi Varshney
  • John Beardall
  • Sankar Bhattacharya
  • Pramod P. WangikarEmail author
Article

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.

Keywords

CO2 tolerance Chlorophyll a fluorescence Physiological stress Non-photochemical quenching PSII heterogeneity Photosynthetic rates 

Notes

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).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10811_2019_1950_MOESM1_ESM.docx (166 kb)
ESM 1 (DOCX 166 kb)

References

  1. Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30:258–270PubMedCrossRefPubMedCentralGoogle Scholar
  2. Antal T, Rubin A (2008) In vivo analysis of chlorophyll a fluorescence induction. Photosynth Res 96:217–226PubMedCrossRefPubMedCentralGoogle Scholar
  3. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113PubMedCrossRefPubMedCentralGoogle Scholar
  4. 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 143:369–377PubMedCrossRefPubMedCentralGoogle Scholar
  5. 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 220:434–446PubMedCrossRefPubMedCentralGoogle Scholar
  6. Bhola VK, Swalaha FM, Nasr M, Kumari S, Bux F (2016) Physiological responses of carbon-sequestering microalgae to elevated carbon regimes. Eur J Phycol 51:401–412CrossRefGoogle Scholar
  7. Black MT, Brearley TH, Horton P (1986) Heterogeneity in chloroplast photosystem II. Photosynth Res 8:193–207PubMedCrossRefPubMedCentralGoogle Scholar
  8. 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 99:3389–3396PubMedCrossRefPubMedCentralGoogle Scholar
  9. 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 100:833–838PubMedCrossRefPubMedCentralGoogle Scholar
  10. 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 102:9135–9142PubMedCrossRefPubMedCentralGoogle Scholar
  11. 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 1–17Google Scholar
  12. Dao LHT, Beardall J (2016a) Effects of lead on two green microalgae Chlorella and Scenedesmus: photosystem II activity and heterogeneity. Algal Res 16:150–159CrossRefGoogle Scholar
  13. Dao LHT, Beardall J (2016b) Effects of lead on growth, photosynthetic characteristics and production of reactive oxygen species of two freshwater green algae. Chemosphere 147:420–429PubMedCrossRefPubMedCentralGoogle Scholar
  14. De Marchin T, Ghysels B, Nicolay S, Franck F (2014) Analysis of PSII antenna size heterogeneity of Chlamydomonas reinhardtii during state transitions. BBA-Bioenergetics 1837:121–130PubMedCrossRefPubMedCentralGoogle Scholar
  15. Eilers PHC, Peeters JCH (1988) A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol Model 42:199–215CrossRefGoogle Scholar
  16. 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 100:685–691PubMedPubMedCentralCrossRefGoogle Scholar
  17. Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131PubMedCrossRefPubMedCentralGoogle Scholar
  18. Guenther JE, Melis A (1990) The physiological significance of photosystem II heterogeneity in chloroplasts. Photosynth Res 23:105–109PubMedCrossRefPubMedCentralGoogle Scholar
  19. Henley WJ (1993) Measurement and interpretatiom of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. J Phycol 29:729–739CrossRefGoogle Scholar
  20. 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 31:674CrossRefGoogle Scholar
  21. Ihnken S, Kromkamp JC, Beardall J (2011) Photoacclimation in Dunaliella tertiolecta reveals a unique NPQ pattern upon exposure to irradiance. Photosynth Res 110:123–137PubMedPubMedCentralCrossRefGoogle Scholar
  22. 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 36:327–332CrossRefGoogle Scholar
  23. 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 21:1569–1574CrossRefGoogle Scholar
  24. 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 122:121–158PubMedPubMedCentralCrossRefGoogle Scholar
  25. 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 28:1509–1520CrossRefGoogle Scholar
  26. 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 680:336–342CrossRefGoogle Scholar
  27. 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 68:2474–2492PubMedPubMedCentralCrossRefGoogle Scholar
  28. 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 57:653–660PubMedCrossRefPubMedCentralGoogle Scholar
  29. 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 19:30–38CrossRefGoogle Scholar
  30. 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 252:344–351PubMedCrossRefPubMedCentralGoogle Scholar
  31. Makino A, Mae T (1999) Photosynthesis and plant growth at elevated levels of CO2. Plant Cell Physiol 40:999–1006CrossRefGoogle Scholar
  32. 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 16:449–457CrossRefGoogle Scholar
  33. 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 26:84–92CrossRefGoogle Scholar
  34. 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 277–292CrossRefGoogle Scholar
  35. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51:659–668CrossRefGoogle Scholar
  36. 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 10:515–525CrossRefGoogle Scholar
  37. Mende D (1980) Evidence for a cyclic PS-II-electron transport in vivo. Plant Sci Lett 17:215–220CrossRefGoogle Scholar
  38. Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566PubMedPubMedCentralCrossRefGoogle Scholar
  39. 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 83:461–465CrossRefGoogle Scholar
  40. 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 7:241–246CrossRefGoogle Scholar
  41. Nedbal L, Trtílek M, Kaftan D (1999) Flash fluorescence induction: a novel method to study regulation of photosystem II. J Photochem Photobiol B Biol 48:154–157CrossRefGoogle Scholar
  42. Pierangelini M, Stojkovic S, Orr PT, Beardall J (2014a) Photosynthetic characteristics of two Cylindrospermopsis raciborskii strains differing in their toxicity. J Phycol 50:292–302PubMedCrossRefPubMedCentralGoogle Scholar
  43. 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 171:1091–1098PubMedCrossRefPubMedCentralGoogle Scholar
  44. 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 38:721–729CrossRefGoogle Scholar
  45. Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat Bot 82:222–237CrossRefGoogle Scholar
  46. Raven JA, Beardall J, Giordano M (2014) Energy costs of carbon dioxide concentrating mechanisms in aquatic organisms. Photosynth Res 121:111–124PubMedCrossRefPubMedCentralGoogle Scholar
  47. Ruban AV, Johnson MP, Duffy CDP (2011) Natural light harvesting: principles and environmental trends. Energy Environ Sci 4:1643–1650CrossRefGoogle Scholar
  48. 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,Google Scholar
  49. Sebök S, Herppich WB, Hanelt D (2017) Red alga Palmaria palmata—growth rate and photosynthetic performance under elevated CO2 treatment. J Appl Phycol 29:381–393CrossRefGoogle Scholar
  50. Seth JR, Wangikar PP (2015) Challenges and opportunities for microalgae-mediated CO2 capture and biorefinery. Biotechnol Bioeng 112:1281–1296PubMedCrossRefPubMedCentralGoogle Scholar
  51. 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 5:169–176PubMedCrossRefPubMedCentralGoogle Scholar
  52. Stirbet A, Govindjee SBJ, Strasser RJ (1998) Chlorophyll a fluorescence induction in higher plants: modelling and numerical simulation. J Theor Biol 193:131–151CrossRefGoogle Scholar
  53. Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plant and cyanobacteria. Photochem Photobiol 61:32–42CrossRefGoogle Scholar
  54. 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 321–362CrossRefGoogle Scholar
  55. 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 76:949–953Google Scholar
  56. Varshney P, Mikulic P, Vonshak A, Beardall J, Wangikar PP (2015) Extremophilic micro-algae and their potential contribution in biotechnology. Bioresour Technol 184:363–372PubMedPubMedCentralCrossRefGoogle Scholar
  57. 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 28:2631–2640CrossRefGoogle Scholar
  58. 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 30:28–37CrossRefGoogle Scholar
  59. Vincent WF, Roy S (1993) Solar ultraviolet-B radiation and aquatic primary production: Damage, protection, and recovery. Environ Rev 1:1–12CrossRefGoogle Scholar
  60. Vinet L, Zhedanov A (2011) A ‘missing’ family of classical orthogonal polynomials. J Phys A Math Theor 44:085201CrossRefGoogle Scholar
  61. Yang Y, Gao K (2003) Effects of CO2 concentrations on the freshwater microalgae, Chlamydomonas reinhardtii, Chlorella pyrenoidosa and Scenedesmus obliquus (Chlorophyta). J Appl Phycol 15:379–389CrossRefGoogle Scholar
  62. 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 82:351–354CrossRefGoogle Scholar
  63. 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 22:479–488CrossRefGoogle Scholar
  64. 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 167:951–958PubMedCrossRefPubMedCentralGoogle Scholar
  65. 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 36:2278–2284PubMedCrossRefPubMedCentralGoogle Scholar
  66. 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 175:556–564CrossRefGoogle Scholar
  67. Zhao B, Su Y, Zhang Y, Cui G (2015) Carbon dioxide fixation and biomass production from combustion flue gas using energy microalgae. Energy 89:347–357CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Prachi Varshney
    • 1
    • 2
    • 3
    • 4
  • John Beardall
    • 3
  • Sankar Bhattacharya
    • 4
  • Pramod P. Wangikar
    • 2
    • 5
    • 6
    Email author
  1. 1.IITB-Monash Research AcademyIndian Institute of Technology BombayMumbaiIndia
  2. 2.Department of Chemical EngineeringIndian Institute of Technology BombayMumbaiIndia
  3. 3.School of Biological SciencesMonash UniversityMelbourneAustralia
  4. 4.Department of Chemical EngineeringMonash UniversityMelbourneAustralia
  5. 5.DBT-Pan IIT Centre for BioenergyIndian Institute of Technology BombayMumbaiIndia
  6. 6.Wadhwani Research Centre for BioengineeringIndian Institute of Technology BombayMumbaiIndia

Personalised recommendations