Comparison of the photosynthetic yield of cyanobacteria and green algae: Different methods give different answers

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Schuurmans, R Milou ^a   Van Alphen, Pascal ^a   Schuurmans, J Merijn ^b   Matthijs, Hans C P ^b   Hellingwerf, Klaas J ^a,c  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c Photanol BV   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMASS; CHLORELLA SOROKINIANA; CONTINUOUS CULTURE; CONTROLLED STUDY; CYANOBACTERIUM; FLUORESCENCE; GREEN ALGA; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYCOBILISOME; PLANT YIELD; QUANTUM YIELD; RESPIRATORY CHAIN; SPECIES; SYNECHOCYSTIS; CHLORELLA; COMPARATIVE STUDY; ELECTRON TRANSPORT; FLUOROMETRY; LIGHT; MASS SPECTROMETRY; METABOLISM; OXIDATION REDUCTION REACTION; OXYGEN CONSUMPTION; PHOTON; PHOTOTROPHY; PHYSIOLOGY; PROCEDURES; RADIATION RESPONSE;

CHLOROPHYLL; CHLOROPHYLL A; PHYCOBILISOME;

BIOMASS; CHLORELLA; CHLOROPHYLL; ELECTRON TRANSPORT; FLUORESCENCE; FLUOROMETRY; LIGHT; MASS SPECTROMETRY; OXIDATION-REDUCTION; OXYGEN CONSUMPTION; PHOTONS; PHOTOSYNTHESIS; PHOTOTROPHIC PROCESSES; PHYCOBILISOMES; SYNECHOCYSTIS;

EID: 84947734625     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0139061     Document Type: Article

References (75)

1. Lewis NS, Nocera DG. Powering the planet: Chemical challenges in solar energy utilization. Proc Natl Acad Sci U S A. 2006; 103: 15729-15735. PMID: 17043226
2. 2 and water based on the 'photanol'approach. J Biotechnol. 2009; 142: 87-90. doi: 10.1016/j.jbiotec.2009.02.002 PMID: 19480951
3. Janssen M, Tramper J, Mur LR, Wijffels RH. Enclosed outdoor photobioreactors: Light regime, photosynthetic efficiency, scale-up, and future prospects. Biotechnol Bioeng. 2003; 81: 193-210. PMID: 12451556
4. 2 sequestration addressing global warming using green algae and cyanobacteria. Bioresour Technol. 2011; 102: 4945-4953. doi: 10.1016/j.biortech.2011.01.054 PMID: 21334885
5. Grobbelaar JU. Microalgal biomass production: Challenges and realities. Photosynthesis Res. 2010; 106: 135-144.
6. Langner U, Jakob T, Stehfest K, Wilhelm C. An energy balance from absorbed photons to new biomass for Chlamydomonas reinhardtii and Chlamydomonas acidophila under neutral and extremely acidic growth conditions. Plant, Cell Environ. 2009; 32: 250-258.
7. Mulders KJM, Lamers PP, Wijffels RH, Martens DE. Dynamics of biomass composition and growth during recovery of nitrogen-starved Chromochloris zofingiensis. Appl Microbiol Biotechnol. 2014: 1-12.
8. Maxwell K, Johnson GN. Chlorophyll fluorescence-A practical guide. J Exp Bot. 2000; 51: 659-668. PMID: 10938857
9. Baker NR, Rosenqvist E. Applications of chlorophyll fluorescence can improve crop production strategies: An examination of future possibilities. J Exp Bot. 2004; 55: 1607-1621. PMID: 15258166
10. 2-limited conditions. Plant Physiol. 2015; 167: 472-480. doi: 10.1104/pp.114. 249987 PMID: 25540330
11. AdamsWWIII, Demmig-Adams B, Winter K, Schreiber U. The ratio of variable to maximum chlorophyll fluorescence from photosystem II, measured in leaves at ambient temperature and at 77K, as an indicator of the photon yield of photosynthesis. Planta. 1990; 180: 166-174. doi: 10.1007/BF00193991 PMID: 24201940
12. Lu C, Zhang J. Effects of water stress on photosystem II photochemistry and its thermostability in wheat plants. J Exp Bot. 1999; 50: 1199-1206.
13. Germ M, Kreft I, Osvald J. Influence of UV-B exclusion and selenium treatment on photochemical efficiency of photosystem II, yield and respiratory potential in pumpkins (cucurbita pepo L.). Plant physiology and Biochemistry. 2005; 43: 445-448. PMID: 15949721
14. Masojídek J, Vonshak A, Torzillo G. Chlorophyll fluorescence applications in microalgal mass cultures. In: Anonymous Chlorophyll a Fluorescence in Aquatic Sciences: Methods and Applications.: Springer; 2010. pp. 277-292.
15. Young EB, Beardall J. Photosynthetic function in Dunaliella tertiolecta (chlorophyta) during a nitrogen starvation and recovery cycle. J Phycol. 2003; 39: 897-905.
16. Gao K, Yu H, Brown MT. Solar PAR and UV radiation affects the physiology and morphology of the cyanobacterium Anabaena sp. PCC 7120. Journal of Photochemistry and Photobiology B: Biology. 2007; 89: 117-124.
17. Allahverdiyeva Y, Mustila H, Ermakova M, Bersanini L, Richaud P, Ajlani G, et al. Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light. Proc Natl Acad Sci U S A. 2013; 110: 4111-4116. doi: 10.1073/pnas.1221194110 PMID: 23431195
18. Schreiber U, Endo T, Mi H, Asada K. Quenching analysis of chlorophyll fluorescence by the saturation pulse method: Particular aspects relating to the study of eukaryotic algae and cyanobacteria. Plant and Cell Physiology. 1995; 36: 873-882.
19. Campbell D, Hurry V, Clarke AK, Gustafsson P, Öquist G. Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol Rev. 1998; 62: 667-683. PMID: 9729605
20. Papageorgiou GC, Tsimilli-Michael M, Stamatakis K. The fast and slow kinetics of chlorophyll a fluorescence induction in plants, algae and cyanobacteria: A viewpoint. Photosynthesis Res. 2007; 94: 275-290.
21. Deblois CP, Marchand A, Juneau P. Comparison of photoacclimation in twelve freshwater photoautotrophs (chlorophyte, bacillaryophyte, cryptophyte and cyanophyte) isolated from a natural community. Plos One. 2013; 8: E57139. doi: 10.1371/Journal.pone.0057139 PMID: 23526934
22. Schreiber U, Schliwa U, Bilger W. Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Res. 1986; 10: 51-62.
23. Mi H, Endo T, Ogawa T, Asada K. Thylakoid membrane-bound, NADPH-specific pyridine nucleotide dehydrogenase complex mediates cyclic electron transport in the cyanobacterium Synechocystis sp. PCC 6803. Plant and Cell Physiology. 1995; 36: 661-668.
24. Yeremenko N, Jeanjean R, Prommeenate P, Krasikov V, Nixon PJ, Vermaas WFJ, et al. Open reading frame ssr2016 is required for antimycin A-sensitive photosystem I-driven cyclic electron flow in the cyanobacterium Synechocystis sp PCC 6803. Plant and Cell Physiology. 2005; 46: 1433-1436. PMID: 15946981
25. Schreiber U. Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: An overview. In: Anonymous Chlorophyll a Fluorescence.: Springer; 2004. pp. 279-319.
26. van Kooten O, Snel JFH. The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Res. 1990; 25: 147-150.
27. Zhu XG, Baker NR, Ort DR, Long SP. Chlorophyll a fluorescence induction kinetics in leaves predicted from a model describing each discrete step of excitation energy and electron transfer associated with photosystem II. Planta. 2005; 223: 114-133. PMID: 16411287
28. Lawson T, Davey PA, Yates SA, Bechtold U, Baeshen M, Baeshen N, et al. C3 photosynthesis in the desert plant Rhazya stricta is fully functional at high temperatures and light intensities. New Phytol. 2014; 201: 862-873. doi: 10.1111/nph.12559 PMID: 24164092
29. Matthijs HCP, Luderus EME, Loffler HJM, Scholts MJC, Kraayenhof R. Energy-metabolism in the cyanobacterium Plectonema boryanum-participation of the thylakoid photosynthetic electron-transfer chain in the dark respiration of NADPH and NADH. Biochim Biophys Acta. 1984; 766: 29-37.
30. Jans F, Mignolet E, Houyoux PA, Cardol P, Ghysels B, Cuine S, et al. A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. Proc Natl Acad Sci U S A. 2008; 105: 20546-20551. doi: 10.1073/pnas.0806896105 PMID: 19074271
31. Schuurmans RM, Schuurmans JM, Bekker M, Kromkamp JC, Matthijs HCP, Hellingwerf KJ. The redox potential of the plastoquinone pool of the cyanobacterium Synechocystis species strain PCC 6803 is under strict homeostatic control. Plant Physiol. 2014; 165: 463-475. doi: 10.1104/pp.114.237313 PMID: 24696521
32. Genty B, Harbinson J, Baker NR. Relative quantum efficiencies of the two photosystems of leaves in photorespiratory and non-respiratory conditions. Plant Physiology and Biochemistry (Paris). 1990; 28: 1-10.
33. Pfündel E. Estimating the contribution of photosystem I to total leaf chlorophyll fluorescence. Photosynthesis Res. 1998; 56: 185-195.
34. Helman Y, Tchernov D, Reinhold L, Shibata M, Ogawa T, Schwarz R, et al. Genes encoding a-type flavoproteins are essential for photoreduction of O2 in cyanobacteria. Current Biology. 2003; 13: 230-235. PMID: 12573219
35. Page LE, Liberton M, Pakrasi HB. Reduction of photoautotrophic productivity in the cyanobacterium Synechocystis sp. strain PCC 6803 by phycobilisome antenna truncation. Appl Environ Microbiol. 2012; 78: 6349-6351. doi: 10.1128/AEM.00499-12 PMID: 22706065
36. Lea-Smith DJ, Bombelli P, Dennis JS, Scott SA, Smith AG, Howe CJ. Phycobilisome-deficient strains of Synechocystis sp. PCC 6803 have reduced size and require carbon-limiting conditions to exhibit enhanced productivity. Plant Physiol. 2014; 165: 705-714. PMID: 24760817
37. Kok B. On the interrelation of respiration and photosynthesis in green plants. Biochim Biophys Acta. 1949; 3: 625-631.
38. Sharp RE, Matthews MA, Boyer JS. Kok effect and the quantum yield of photosynthesis: Light partially inhibits dark respiration. Plant Physiol. 1984; 75: 95-101. PMID: 16663610
39. Kana TM. Light-dependent oxygen cycling measured by an O18 isotope-dilution technique. Mar Ecol Prog Ser. 1990; 64: 293-300.
40. Allen J, Asada K, Foyer CH, Matthijs HCP. The water-water cycle as alternative photon and electron sinks-discussion. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences. 2000; 355: 1430-1431.
41. Helman Y, Barkan E, Eisenstadt D, Luz B, Kaplan A. Fractionation of the three stable oxygen isotopes by oxygen-producing and oxygen-consuming reactions in photosynthetic organisms. Plant Physiol. 2005; 138: 2292-2298. PMID: 16040650
42. Huisman J, Matthijs HCP, Visser PM, Balke H, Sigon CAM, Passarge J, et al. Principles of the light-limited chemostat: Theory and ecological applications. Antonie Van Leeuwenhoek. 2002; 81: 117-133. PMID: 12448711
43. Wang Y, Li Y, Shi D, Shen G, Ru B, Zhang S. Characteristics of mixotrophic growth of Synechocystis sp. in an enclosed photobioreactor. Biotechnol Lett. 2002; 24: 1593-1597.
44. Shastri AA, Morgan JA. Flux balance analysis of photoautotrophic metabolism. Biotechnol Prog. 2005; 21: 1617-1626. PMID: 16321043
45. Kim HW, Vannela R, Zhou C, Harto C, Rittmann BE. Photoautotrophic nutrient utilization and limitation during semi-continuous growth of Synechocystis sp. PCC6803. Biotechnol Bioeng. 2010; 106: 553-563. doi: 10.1002/bit.22724 PMID: 20340142
46. Phukan MM, Chutia RS, Konwar B, Kataki R. Microalgae Chlorella as a potential bio-energy feedstock. Appl Energy. 2011; 88: 3307-3312.
47. Wang K, Brown RC. Catalytic pyrolysis of microalgae for production of aromatics and ammonia. Green Chem. 2013; 15: 675-681.
48. Dong X, Chen Z, Xue S, Zhang J, Zhou J, Liu Y, et al. Catalytic pyrolysis of microalga Chlorella pyrenoidosa for production of ethylene, propylene and butene. RSC Advances. 2013; 3: 25780-25787.
49. Genty B, Briantais JM, Baker NR. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta (BBA)-General Subjects. 1989; 990: 87-92.
50. Fork DC, Satoh K. State I-state-II transitions in the thermophilic blue-green-alga (cyanobacterium) Synechococcus lividus. Photochem Photobiol. 1983; 37: 421-427.
51. Wilson A, Ajlani G, Verbavatz JM, Vass I, Kerfeld CA, Kirilovsky D. A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell. 2006; 18: 992-1007. PMID: 16531492
52. Acuña AM, Snellenburg JJ, Gwizdala M, Kirilovsky D, van Grondelle R, van Stokkum IH. Resolving the contribution of the uncoupled phycobilisomes to cyanobacterial pulse-amplitude modulated (PAM) fluorometry signals. Photosynthesis Res. 2015: 1-12.
53. Campbell D, Öquist G. Predicting light acclimation in cyanobacteria from nonphotochemical quenching of photosystem II fluorescence, which reflects state transitions in these organisms. Plant Physiol. 1996; 111: 1293-1298. PMID: 12226362
54. Velitchkova MY, Picorel R. Photobleaching of photosynthetic pigments in spinach thylakoid membranes. effect of temperature, oxygen and DCMU. Biophys Chem. 2004; 107: 25-32. PMID: 14871598
55. Laczkó-Dobos H, Ughy B, Tóth SZ, Komenda J, Zsiros O, Domonkos I, et al. Role of phosphatidylglycerol in the function and assembly of photosystem II reaction center, studied in a cdsA-inactivated PAL mutant strain of Synechocystis sp. PCC6803 that lacks phycobilisomes. Biochimica et Biophysica Acta (BBA)-Bioenergetics. 2008; 1777: 1184-1194.
56. Nagarajan A, Page LE, Liberton M, Pakrasi HB. Consequences of decreased light harvesting capability on photosystem II function in Synechocystis sp. PCC 6803. Life. 2014; 4: 903-914. doi: 10.3390/life4040903 PMID: 25513759
57. Demmig-Adams B, AdamsWWIII, Czygan FC, Schreiber U, Lange OL. Differences in the capacity for radiationless energy dissipation in the photochemical apparatus of green and blue-green algal lichens associated with differences in carotenoid composition. Planta. 1990; 180: 582-589. doi: 10.1007/BF02411457 PMID: 24202104
58. Kirilovsky D, Kerfeld CA. The orange carotenoid protein in photoprotection of photosystem II in cyanobacteria. Biochimica et Biophysica Acta (BBA)-Bioenergetics. 2012; 1817: 158-166.
59. Scheffer M, Rinaldi S, Gragnani A, Mur LR, van Nes EH. On the dominance of filamentous cyanobacteria in shallow, turbid lakes. Ecology. 1997; 78: 272-282.
60. Passarge J, Hol S, Escher M, Huisman J. Competition for nutrients and light: Stable coexistence, alternative stable states, or competitive exclusion? Ecol Monogr. 2006; 76: 57-72.
61. Agawin NSR, Rabouille S, Veldhuis MJW, Servatius L, Hol S, van Overzee HMJ, et al. Competition and facilitation between unicellular nitrogen-fixing cyanobacteria and non-nitrogen-fixing phytoplankton species. Limnol Oceanogr. 2007; 52: 2233-2248.
62. Kirst H, Formighieri C, Melis A. Maximizing photosynthetic efficiency and culture productivity in cyanobacteria upon minimizing the phycobilisome light-harvesting antenna size. Biochimica et Biophysica Acta (BBA)-Bioenergetics. 2014; 1837: 1653-1664.
63. Schubert H, Matthijs HCP, Mur LR. In vivo assay of P700 redox changes in the cyanobacterium Fremyella diplosiphon and the role of cytochrome c oxidase in regulation of photosynthetic electron transfer. Photosynthetica. 1995; 31: 517-527.
64. Scholes P, Mitchell P, Moyle J. The polarity of proton translocation in some photosynthetic microorganisms. European Journal of Biochemistry. 1969; 8: 450-454. PMID: 5802881
65. Kana TM. Relationship between photosynthetic oxygen cycling and carbon assimilation in Synechococcus Wh7803 (cyanophyta). J Phycol. 1992; 28: 304-308.
66. Matthijs HCP, Luderus EME, Scholts MJC, Kraayenhof R. Energy-metabolism in the cyanobacterium Plectonema boryanum-oxidative-phosphorylation and respiratory pathways. Biochim Biophys Acta. 1984; 766: 38-44.
67. Scherer S, Alpes I, Sadowski H, Böger P. Ferredoxin-NADP oxidoreductase is the respiratory NADPH dehydrogenase of the cyanobacterium Anabaena variabilis. Arch Biochem Biophys. 1988; 267: 228-235. PMID: 2461678
68. 2, but a green E. coli. Frontiers in bioengineering and biotechnology. 2014; 2.
69. Torzillo G, Pushparaj B, Masojidek J, Vonshak A. Biological constraints in algal biotechnology. Biotechnology and bioprocess engineering. 2003; 8: 338-348.
70. Howitt CA, Vermaas WFJ. Quinol and cytochrome oxidases in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry (N Y). 1998; 37: 17944-17951.
71. Mi H, Endo T, Schreiber U, Ogawa T, Asada K. Electron donation from cyclic and respiratory flows to the photosynthetic intersystem chain is mediated by pyridine nucleotide dehydrogenase in the cyanobacterium Synechocystis PCC 6803. Plant and cell physiology. 1992; 33: 1233-1237.
72. Allahverdiyeva Y, Ermakova M, Eisenhut M, Zhang P, Richaud P, Hagemann M, et al. Interplay between flavodiiron proteins and photorespiration in Synechocystis sp. PCC 6803. J Biol Chem. 2011; 286: 24007-24014. doi: 10.1074/jbc.M111.223289 PMID: 21602273
73. Ajlani G, Vernotte C. Construction and characterization of a phycobiliprotein-less mutant of Synechocystis sp. PCC 6803. Plant Mol Biol. 1998; 37: 577-580. PMID: 9617824
74. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol. 1979; 111: 1-61.
75. Kana TM, Darkangelo C, Hunt MD, Oldham JB, Bennett GE, Cornwell JC. Membrane inlet mass-spectrometer for rapid high-precision determination of N2, O2, and ar in environmental water samples. Anal Chem. 1994; 66: 4166-4170.