Exploiting algal NADPH oxidase for biophotovoltaic energy

Plant Biotechnology Journal

Volumn 14, Issue 1, 2016, Pages 22-28

  Anderson, Alexander ^a   Laohavisit, Anuphon ^a,c   Blaby, Ian K ^b   Bombelli, Paolo ^a   Howe, Christopher J ^a   Merchant, Sabeeha S ^b   Davies, Julia M ^a   Smith, Alison G ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c RIKEN   (Japan)

Author keywords

Chlamydomonas; Alga; Biophotovoltaic; Energy; NADPH oxidase

Indexed keywords

BIOFUEL; PLANT PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE;

CHEMISTRY; CHLAMYDOMONAS REINHARDTII; ELECTRICITY; ENZYMOLOGY; EXTRACELLULAR SPACE; GENETIC COMPLEMENTATION; LIGHT; METABOLISM; RADIATION RESPONSE;

BIOFUELS; CHLAMYDOMONAS REINHARDTII; ELECTRICITY; EXTRACELLULAR SPACE; GENETIC COMPLEMENTATION TEST; LIGHT; NADPH OXIDASE; PLANT PROTEINS; SUPEROXIDES;

EID: 84954546508     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12332     Document Type: Article

References (43)

1. Allen, M.D., del Campo, J.A., Kropat, J. and Merchant, S.S. (2007) FEA1, FEA2, and FRE1, encoding two homologous secreted proteins and a candidate ferrireductase, are expressed coordinately with FOX1 and FTR1 in iron-deficient Chlamydomonas reinhardtii. Eukaryot. Cell 6, 1841-1852.
2. Anderson, A., Bothwell, J.H., Laohavisit, A., Smith, A.G. and Davies, J.M. (2011) NOX or not? Evidence for algal NADPH oxidases. Trends Plant Sci. 16, 579-581.
3. Blaby, I.K., Glaesner, A.G., Mettler, T., Fitz-Gibbon, S.T., Gallaher, S.D., Liu, B.S., Boyle, N.R., Kropat, J., Stitt, M., Johnson, S., Benning, C., Pellegrini, M., Casero, D. and Merchant, S.S. (2013) Systems-level analysis of nitrogen starvation-induced modifications of carbon metabolism in a Chlamydomonas reinhardtii starchless mutant. Plant Cell, 25, 4305-4323.
4. Bombelli, P., Bradley, R.W., Scott, A.M., Philips, A.J., McCormick, A.J., Cruz, S.M., Anderson, A.A., Yunus, K., Bendall, D.S., Cameron, P., Davies, J.M., Smith, A.G., Howe, C.J. and Fisher, A.C. (2011) Quantitative analysis of the factors limiting solar power transduction by Synechocystis sp. PCC 6803 in biological photovoltaic devices. Energy Environ. Sci. 4, 4690-4698.
5. Bouarab, K. (1999) Sulfated oligosaccharides mediate the interaction between a marine red alga and its green algal pathogenic endophyte. Plant Cell, 11, 1635-1650.
6. Bradley, R.W., Bombelli, P., Rowden, S.J.L. and Howe, C.J. (2012) Biological photovoltaics: intra- and extra-cellular electron transport by cyanobacteria. Biochem. Soc. Trans. 40, 1302-1307.
7. Cho, A. (2010) Energy's tricky tradeoffs. Science, 329, 786-787.
8. 2+-interdependent, reactive oxygen species gradient is associated with polarized growth in Fucus serratus zygotes. Planta, 227, 1037-1046.
9. Davies, D.R. and Plaskitt, A. (1971) Genetic and structural analyses of cell-wall formation in Chlamydomonas reinhardtii. Genet. Res. 17, 33-43.
10. Fischer, N. and Rochaix, J.D. (2001) The flanking regions of PsaD drive efficient gene expression in the nucleus of the green alga Chlamydomonas reinhardtii. Mol. Genet. Genomics, 265, 888-894.
11. Foreman, J., Demidchik, V., Bothwell, J.H.F., Mylona, P., Miedema, H., Torres, M.A., Linstead, P., Costa, S., Brownlee, C., Jones, J.D.G., Davies, J.M. and Dolan, L. (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature, 422, 442-446.
12. + deficiency inhibits photosynthetic activity through superoxide anion production in protoplasts isolated from the thallus of Ulva pertusa. J. Plant Biol. 53, 155-164.
13. Gonzalez, A., Vera, J., Castro, J., Dennett, G., Mellado, M., Morales, B., Correa, J.A. and Moenne, A. (2010) Co-occurring increases of calcium and organellar reactive oxygen species determine differential activation of antioxidant and defense enzymes in Ulva compressa (Chlorophyta) exposed to copper excess. Plant, Cell Environ. 33, 1627-1640.
14. Hema, R., Senthil-Kumar, M., Shivakumar, S., Chandrasekhara Reddy, P., Udayakumar, M., Shivakumar, R.H.M.S.S. and Udayakumar, P.C.R.M. (2007) Chlamydomonas reinhardtii, a model system for functional validation of abiotic stress responsive genes. Cultures, 226, 655-670.
15. Hemschemeier, A., Casero, D., Liu, B., Benning, C., Pellegrini, M., Happe, T. and Merchant, S.S. (2013) COPPER RESPONSE REGULATOR1-dependent and -independent responses of the Chlamydomonas reinhardtii transcriptome to dark anoxia. Plant Cell, 25, 3186-3211.
16. Hervé, C., Tonon, T., Collén, J., Corre, E. and Boyen, C. (2005) NADPH oxidases in Eukaryotes: red algae provide new hints!. Curr. Genet. 49, 190-204.
17. Inskeep, W.P. and Bloom, P.R. (1985) Extinction coefficients of chlorophyll a and b in n, n-dimethylformamide and 80% acetone. Plant Physiol. 77, 483-485.
18. Jones, C.S. and Mayfield, S.P. (2012) Algae biofuels: versatility for the future of bioenergy. Curr. Opin. Biotechnol. 23, 346-351.
19. Kadota, Y., Sklenar, J., Derbyshire, P., Stransfeld, L., Asai, S., Ntoukakis, V., Jones, J.D.G., Shirasu, K., Menke, F., Jones, A. and Zipfel, C. (2014) Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell 54, 43-55.
20. Kawahara, B., Quinn, M.T. and Lambeth, J.D. (2007) Molecular evolution of the reactive oxygen-generating NADPH oxidase (Nox/Duox) family of enzymes. BMC Evol. Biol. 7, 109.
21. Kim, D., Watanabe, M., Nakayasu, Y. and Kohata, K. (2004) Production of superoxide anion and hydrogen peroxide associated with cell growth of Chattonella antiqua. Aquat. Microb. Ecol. 35, 57-64.
22. Kim, D., Nakashima, T., Matsuyama, Y., Niwano, Y., Yamaguchi, K. and Oda, T. (2007) Presence of the distinct systems responsible for superoxide anion and hydrogen peroxide generation in red tide phytoplankton Chattonella marina and Chattonella ovata. J. Plankton Res. 29, 241-247.
23. Küpper, F.C., Kloareg, B., Guern, J. and Potin, P. (2001) Oligoguluronates elicit an oxidative burst in the brown algal kelp Laminaria digitata. Plant Physiol. 125, 278-291.
24. Larkum, A.W.D. (2010) Limitations and prospects of natural photosynthesis for bioenergy production. Curr. Opin. Biotechnol. 21, 271-276.
25. Lee, Y., Rubio, M.C., Alassimone, J. and Geldner, N. (2013) A mechanism for localized lignin deposition in the endodermis. Cell 153, 402-412.
26. Li, Y., Han, D.X., Hu, G.R., Dauvillee, D., Sommerfeld, M., Ball, S. and Hua, Q. (2010) Chlamydomonas starchless mutant defective in ADP-glucose pyrophosphorylase hyper-accumulates triacylglycerol. Metab. Eng. 12, 387-391.
27. Liu, F. and Pang, S.J. (2010) Stress tolerance and antioxidant enzymatic activities in the metabolisms of the reactive oxygen species in two intertidal red algae Grateloupia turuturu and Palmaria palmata. J. Exp. Mar. Bio. Ecol. 382, 82-87.
28. Marshall, J.-A., Ross, T., Pyecroft, S., Hallegraeff, G., Salas, M. and Oda, T. (2005) Superoxide production by marine microalgae. Mar. Biol. 147, 533-540.
29. McCormick, A.J., Bombelli, P., Scott, A.M., Philips, A.J., Smith, A.G., Fisher, A.C. and Howe, C.J. (2011) Photosynthetic biofilms in pure culture harness solar energy in a mediatorless bio-photovoltaic cell (BPV) system. Energy Environ. Sci. 4, 4699.
30. Oda, T., Moritomi, J., Kawano, I., Hamaguchi, S., Ishimatsu, A. and Muramatsu, T. (1995) Catalase- and superoxide dismutase-induced morphological changes and growth inhibition in the red tide phytoplankton Chattonella marina. Biosci. Biotechnol. Biochem. 59, 2044-2048.
31. Pérez-Pérez, M.E., Couso, I. and Crespo, J.L. (2012) Carotenoid deficiency triggers autophagy in the model green alga Chlamydomonas reinhardtii. Autophagy, 8, 376-388.
32. Pröschold, T., Harris, E.H. and Coleman, A.W. (2005) Portrait of a species: Chlamydomonas reinhardtii. Genetics, 170, 1601-1610.
33. Rosenbaum, M., He, Z. and Angenent, L.T. (2010) Light energy to bioelectricity: photosynthetic microbial fuel cells. Curr. Opin. Biotechnol. 21, 259-264.
34. Ross, C., Küpper, F.C., Vreeland, V., Herbert Waite, J. and Jacobs, R.S. (2005) Evidence of a latent oxidative burst in relation to wound repair in the giant unicellular chlorophytes Dasycladus vermicularis. J. Phycol. 41, 531-541.
35. Sagi, M., Davydov, O., Orazova, S., Yesbergenova, Z., Ophir, R., Stratmann, J.W. and Fluhr, R. (2004) Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. Society, 16, 616-628.
36. Sakai, M., Vonderheit, A., Wei, X., Kuttel, C. and Stemmer, A. (2009) A novel biofuel cell harvesting energy from activated human macrophages. Biosens. Bioelectron. 25, 68-75.
37. Samsonoff, N., Ooms, M. and Sinton, D. (2014) A photosynthetic-plasmonic voltaic cell: excitation of photosynthetic bacteria and current collection through a plasmonic substrate. App. Phys. Lett. 104, 043704.
38. Schrenzel, J., Serrander, L., Bánfi, B., Nüsse, O., Fouyouzi, R., Lew, D.P., Demaurex, N. and Krause, K.H. (1998) Electron currents generated by the human phagocyte NADPH oxidase. Nature, 392, 734-737.
39. Scott, S.A., Davey, M.P., Dennis, J.S., Horst, I., Howe, C.J., Lea-Smith, D. and Smith, A.G. (2010) Biodiesel from algae: challenges and prospects. Curr. Opin. Biotechnol. 21, 277-286.
40. Sutherland, M.W. and Learmonth, B.A. (1997) The tetrazolium dyes MTS and XTT provide new quantitative assays for superoxide and superoxide dismutase. Free Radic. Res. 27, 283-289.
41. Torres, M.A., Onouchi, H., Hamada, S., Machida, C., Hammond-kosack, K.E. and Jones, J.D.G. (1998) Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91 phox). Plant J. 14, 365-370.
42. Voigt, J., Liebich, I., Hinkelmann, B. and Kiees, M. (1996) Immunological identification of a putative precursor of the insoluble glycoprotein framework of the Chlamydomonas cell wall. Plant Cell Physiol. 37, 91-101.
43. Zhu, X.G., Long, S.P. and Ort, D.R. (2010) Improving photosynthetic efficiency for greater yield. Annu. Rev. Plant Biol. 61, 235-261.