Metabolic engineering of the Chl d-dominated cyanobacterium acaryochloris marina: Production of a novel chl species by the introduction of the chlorophyllide a oxygenase gene

Plant and Cell Physiology

Volumn 53, Issue 3, 2012, Pages 518-527

  Tsuchiya, Tohru ^a   Mizoguchi, Tadashi ^b   Akimoto, Seiji ^c   Tomo, Tatsuya ^d,e   Tamiaki, Hitoshi ^b   Mimuro, Mamoru ^a  

^a KYOTO UNIVERSITY   (Japan)

^b RITSUMEIKAN UNIVERSITY   (Japan)

^c KOBE UNIVERSITY   (Japan)

^d TOKYO UNIVERSITY OF SCIENCE   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Acaryochloris marina; Chlorophyllide a oxygenase; Metabolic engineering; Novel Chl; Transformation

Indexed keywords

CHLOROPHYLL; CHLOROPHYLL A OXYGENASE; CHLOROPHYLL D; OXYGENASE;

ARTICLE; BACTERIAL GENE; BACTERIUM CONJUGATION; BIOSYNTHESIS; CHEMISTRY; CYANOBACTERIUM; CYTOLOGY; ENZYMOLOGY; GENE VECTOR; GENETIC TRANSFORMATION; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HOST RANGE; METABOLIC ENGINEERING; METABOLISM; METHODOLOGY; PLASMID; PROCHLOROTHRIX; REPRODUCIBILITY; SPECTROSCOPY;

BIOSYNTHETIC PATHWAYS; CHLOROPHYLL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CONJUGATION, GENETIC; CYANOBACTERIA; GENES, BACTERIAL; GENETIC VECTORS; HOST SPECIFICITY; METABOLIC ENGINEERING; OXYGENASES; PLASMIDS; PROCHLOROTHRIX; REPRODUCIBILITY OF RESULTS; SPECTRUM ANALYSIS; TRANSFORMATION, GENETIC;

ACARYOCHLORIS MARINA;

EID: 84858037720     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcs007     Document Type: Article

References (39)

1. Alexeyev, M.F., Shokolenko, I.N. and Croughan, T.P. (1995) Improved antibiotic-resistance gene cassettes and omega elements for Escherichia coli vector construction and in vitro deletion/insertion mutagenesis. Gene 160: 63-67.
2. Allakhverdiev, S.I., Tomo, T., Shimada, Y., Kindo, H., Nagao, R., Klimov, V.V. et al. (2010) Redox potential of pheophytin a in photosystem II of two cyanobacteria having the different special pair chlorophylls. Proc. Natl Acad. Sci. USA 107: 3924-3929.
3. Allakhverdiev, S.I., Tsuchiya, T., Watabe, K., Kojima, A., Los, D.A., Tomo, T. et al. (2011) Redox potentials of primary electron acceptor quinone molecule (QA)-and conserved energetics of photosystem II in cyanobacteria with chlorophyll a and chlorophyll d. Proc. Natl Acad. Sci. USA 108: 8054-8058.
4. Chen, M. and Blankenship, R.E. (2011) Expanding the solar spectrum used by photosynthesis. Trends Plant Sci. 16: 427-431.
5. Chen, M., Schliep, M., Willows, R.D., Cai, Z.-L., Neilan, B.A. and Scheer, H. (2010) A red-shifted chlorophyll. Science 329: 1318-1319.
6. Elhai, J. and Wolk, C.P. (1988) Conjugal transfer of DNA to cyanobacteria. Methods Enzymol. 167: 747-754.
7. Gomez Maqueo Chew, A. and Bryant, D.A. (2007) Chlorophyll biosynthesis in bacteria: the origins of structural and functional diversity. Annu. Rev. Microbiol. 61: 113-129. (Pubitemid 350058202)
8. Guerry, P., van Embden, J. and Falkow, S. (1974) Molecular nature of two nonconjugative plasmids carrying drug resistance genes. J. Bacteriol. 117: 619-630.
9. Hirashima, M., Satoh, S., Tanaka, R. and Tanaka, A. (2006) Pigment shuffling in antenna systems achieved by expressing prokaryotic chlorophyllide a oxygenase in Arabidopsis. J. Biol. Chem. 281: 15385-15393. (Pubitemid 43855130)
10. Islam, M.R., Aikawa, S., Midorikawa, T., Kashino, Y., Satoh, K. and Koike, H. (2008) slr1923 of Synechocystis sp. PCC6803 is essential for conversion of 3,8-divinyl(proto)chlorophyll(ide) to 3-monovinyl(proto) chlorophyll(ide). Plant Physiol. 148: 1068-1081. (Pubitemid 352847540)
11. Ito, H., Yokono, M., Tanaka, R. and Tanaka, A. (2008) Identification of a novel vinyl reductase gene essential for the biosynthesis of monovinyl chlorophyll in Synechocystis sp. PCC6803. J. Biol. Chem. 283: 9002-9011.
12. Hu, Q., Miyashita, H., Iwasaki, I., Kurano, N., Miyachi, S., Iwaki, M. et al. (1998) A photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis. Proc. Natl Acad. Sci. USA 95: 13319-13323. (Pubitemid 28509569)
13. Kashiyama, Y., Miyashita, H., Ohkubo, S., Ogawa, N.O., Chikaraishi, Y., Takano, Y. et al. (2008) Evidence of global chlorophyll d. Science 321: 658.
14. Kobayashi, M., Akiyama, M., Kano, H. and Kise, H. (2006) Spectroscopy and structure determination. In Chlorophylls and Bacteriochlorophylls: Biochemistry, Biophysics, Functions and Applications. Edited by Grimm, B., Porra, R.J., Rüdiger, W. and Scheer, H. pp. 79-94. Springer, Dordrecht, The Netherlands.
15. Koksharova, O.A. and Wolk, C.P. (2002) Genetic tools for cyanobacteria. Appl. Microbiol. Biotechnol. 58: 123-137.
16. Miyashita, H., Adachi, K., Kurano, N., Ikemoto, H., Chihara, M. and Miyachi, S. (1996) Chlorophyll d as a major pigment. Nature 338: 402. (Pubitemid 26330822)
17. Miyashita, H., Adachi, K., Kurano, N., Ikemoto, H., Chihara, M. and Miyachi, S. (1997) Pigment composition of a novel oxygenic photosynthetic prokaryote containing chlorophyll d as the major chlorophyll. Plant Cell Physiol. 38: 274-281. (Pubitemid 27210900)
18. Miyashita, H., Ikemoto, H., Kurano, N., Miyachi, S. and Chihara, M. (2003) Acaryochloris marina gen. et sp. nov. (cyanobacteria), an oxygenic photosynthetic prokaryote containing Chl d as a major pigment. J. Phycol. 39: 1247-1253. (Pubitemid 38024657)
19. Mizoguchi, T., Harada, J. and Tamiaki, H. (2006) Structural determination of dihydro-and tetrahydrogeranylgeranyl groups at the 17-propionate of bacteriochlorophylls-a. FEBS Lett. 580: 6644-6648. (Pubitemid 44827025)
20. Nagata, N., Satoh, S., Tanaka, R. and Tanaka, A. (2004) Domain structures of chlorophyllide a oxygenase of green plants and Prochlorothrix hollandica in relation to catalytic functions. Planta 218: 1019-1025. (Pubitemid 38504253)
21. Nagata, N., Tanaka, R., Satoh, S. and Tanaka, A. (2005) Identification of a vinyl reductase gene for chlorophyll synthesis in Arabidopsis thaliana and implications for the evolution of Prochlorococcus species. Plant Cell 17: 233-240. (Pubitemid 41672999)
22. Nakanishi, H., Nozue, H., Suzuki, K., Kaneko, Y., Taguchi, G. and Hayashida, N. (2005) Characterization of the Arabidopsis thaliana mutant pcb2 which accumulates divinyl chlorophylls. Plant Cell Physiol. 46: 467-473.
23. Oba, T., Uda, Y., Matsuda, K., Fukusumi, T., Ito, S., Hiratani, K. et al. (2011) A mild conversion from 3-vinyl-to 3-formyl-chlorophyll derivatives. Bioorg. Med. Chem. Lett. 21: 2489-2491.
24. Oster, U., Tanaka, R., Tanaka, A. and Rüdiger, W. (2000) Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. Plant J. 21: 305-310. (Pubitemid 30152769)
25. Partensky, F., Hoepffner, N., Li, W.K.W., Ulloa, O. and Vaulot, D. (1993) Photoacclimation of Prochlorococcus sp. (Prochlorophyta) strains isolated from the North Atlantic and the Mediterranean Sea. Plant Physiol. 101: 285-296.
26. Porra, R.J., Thompson, W.A. and Kriedemann, P.E. (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975: 384-394.
27. Satoh, S., Ikeuchi, M., Mimuro, M. and Tanaka, A. (2001) Chlorophyll b expressed in cyanobacteria functions as a light-harvesting antenna in photosystem I through flexibility of the proteins. J. Biol. Chem. 276: 4293-4297.
28. Satoh, S. and Tanaka, A. (2006) Identification of chlorophyllide a oxygenase in the Prochlorococcus genome by a comparative genomic approach. Plant Cell Physiol. 47: 1622-1629. (Pubitemid 44968257)
29. Schliep, M., Crossett, B., Willows, R.D. and Chen, M. (2010) 18O labeling of chlorophyll d in Acaryochloris marina reveals that chlorophyll a and molecular oxygen are precursors. J. Biol. Chem. 285: 28450-28456.
30. Scholz, P., Haring, V., Wittmann-Liehold, B., Ashman, K., Bagdasarian, M. and Scherzinger, E. (1989) Complete nucleotide sequence and gene organization of the broad-host-range plasmid RSF1010. Gene 75: 271-288. (Pubitemid 19100128)
31. Swingley, W.D., Chen, M., Cheung, P.C., Conrad, A.L., Dejesa, L.C., Hao, J. et al. (2008) Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina. Proc. Natl Acad. Sci. USA 105: 2005-2010. (Pubitemid 351439455)
32. Tamiaki, H., Shibata, R. and Mizoguchi, T. (2007) The 17-propionate function of (bacterio)chlorophylls: biological implication of their long esterifying chains in photosynthetic systems. Photochem. Photobiol. 83: 152-162. (Pubitemid 46697235)
33. Tanaka, A., Ito, H., Tanaka, R., Tanaka, N., Yoshida, K. and Okada, K. (1998) Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc. Natl Acad. Sci. USA 95: 12719-12723. (Pubitemid 28483831)
34. Tomo, T., Kato, Y., Suzuki, T., Akimoto, S., Okubo, T., Noguchi, T. et al. (2008) Characterization of highly purified photosystem I complexes from the chlorophyll d-dominated cyanobacterium Acaryochloris marina MBIC 11017. J. Biol. Chem. 283: 18198-18209.
35. Tomo, T., Okubo, T., Akimoto, S., Yokono, M., Miyashita, H., Tsuchiya, T. et al. (2007) Identification of the special pair of photosystem II in a chlorophyll d-dominated cyanobacterium. Proc. Natl Acad. Sci. USA 104: 7283-7288. (Pubitemid 47186046)
36. Tomo, T., Suzuki, T., Hirano, E., Tsuchiya, T., Miyashita, H., Dohmae, N. et al. (2006) Reversible absorption change of chlorophyll d in solutions. Chem. Phys. Lett. 423: 282-287. (Pubitemid 44250994)
37. Tsuchiya, T., Takaichi, S., Misawa, N., Maoka, T., Miyashita, H. and Mimuro, M. (2005) The cyanobacterium Gloeobacter violaceus PCC 7421 uses bacterial-type phytoene desaturase in carotenoid biosynthesis. FEBS Lett. 579: 2125-2129. (Pubitemid 40469681)
38. Xu, H., Vavilin, D. and Vermaas, W. (2001) Chlorophyll b can serve as the major pigment in functional photosystem II complexes of cyanobacteria. Proc. Natl Acad. Sci. USA 98: 14168-14173. (Pubitemid 33116042)
39. Zapata, M., Rodríguez, F. and Garrid, J.L. (2000) Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Mar. Ecol. Prog. Ser. 195: 29-45. (Pubitemid 30221208)