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Photosynthesis Research

, Volume 139, Issue 1–3, pp 163–171 | Cite as

In vitro demethoxycarbonylation of various chlorophyll analogs by a BciC enzyme

  • Misato Teramura
  • Jiro Harada
  • Hitoshi TamiakiEmail author
Original Article

Abstract

Unique light-harvesting antennas in the green sulfur bacterium Chlorobaculum tepidum, called chlorosomes, consist of self-aggregates of bacteriochlorophyll (BChl) c. In the biosynthesis of BChl c, BciC demethoxycarbonylase removes the C132-methoxycarbonyl group to facilitate the self-aggregation of BChl c. We previously reported the in vitro BciC-enzymatic reactions and discussed the function of this enzyme in the biosynthesis of BChl c. This study aims to examine the substrate specificity of BciC in detail using several semi-synthetic (bacterio)chlorophyll derivatives. The results indicate that the substrate specificity of BciC is measurably affected by structural changes on the A/B rings including the bacteriochlorin π-systems. Moreover, BciC showed its activity on a Zn-chelated chlorophyll derivative. On the contrary, BciC recognized structural modifications on the D/E rings, including porphyrin pigments, which resulted in the significant decrease in the enzymatic activity. The utilization of BciC provides mild conditions that may be useful for the in vitro preparation of various chemically (un)stable chlorophyllous pigments.

Keywords

Bacteriochlorophyll Biosynthesis Chlorosome Demethoxycarbonylase Green sulfur bacterium 

Abbreviations

3Ac

3-Acetyl

BChl

Bacteriochlorophyll

BChlide

Bacteriochlorophyllide

Cba.

Chlorobaculum

Chl

Chlorophyll

Chlide

Chlorophyllide

E.

Escherichia

ESI

Electrospray ionization

3HE

3-(1-Hydroxyethyl)

LCMS

Liquid chromatography–mass spectrometry

PDA

Photodiode array

Pheide

Pheophorbide

RP

Reversed phase

tR

Retention time

3V

3-Vinyl

Notes

Acknowledgements

This work was partially supported by JSPS KAKENHI Grant Number JP17H06436 in the Scientific Research on Innovative Areas “Innovation for Light-Energy Conversion (I4LEC)” (to HT) as well as the Sasakawa Scientific Research Grant from the Japan Science Society and JSPS KAKENHI Grant Number JP17J08860 in the JSPS Research Fellow program (to MT).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11120_2018_573_MOESM1_ESM.docx (188 kb)
Supplementary material 1 (DOCX 188 KB)

References

  1. Blankenship RE, Mastuura K (2003) Antenna complexes from green photosynthetic bacteria. In: Green BR, Parson WW (eds) Light-harvesting antennas in photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 195–217CrossRefGoogle Scholar
  2. Bollivar DW, Jiang ZY, Bauer CE, Beale SI (1994) Heterologous expression of the bchM gene product from Rhodobacter capsulatus and demonstration that it encodes S-adenosyl-l-methionine: Mg-protoporphyrin IX methyltransferase. J Bacteriol 176:5290–5296CrossRefGoogle Scholar
  3. Bryant DA, Costas AMG, Maresca JA, Chew AGM, Klatt CG, Bateson MM, Tallon LJ, Hostetler J, Nelson WC, Heidelberg JF, Ward DM (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic acidobacterium. Science 317:523–526CrossRefGoogle Scholar
  4. Chen GE, Canniffe DP, Barnett SFH, Hollingshead S, Brindley AA, Vasilev C, Bryant DA, Hunter N (2018) Complete enzyme set for chlorophyll biosynthesis in Escherichia coli. Sci Adv 4:eaaq1407CrossRefGoogle Scholar
  5. Gibson LC, Hunter CN (1994) The bacteriochlorophyll biosynthesis gene, bchM, of Rhodobacter sphaeroides encodes S-adenosyl-l-methionine: Mg protoporphyrin IX methyltransferase. FEBS Lett 352:127–130CrossRefGoogle Scholar
  6. Griffiths WT (1980) Substrate-specificity studies on protochlorophyllide reductase in barley (Hordeum vulgare) etioplast membranes. Biochem J 186:267–278CrossRefGoogle Scholar
  7. Harada J, Teramura M, Mizoguchi T, Tsukatani Y, Yamamoto K, Tamiaki H (2015) Stereochemical conversion of the 3-vinyl group to 1-hydroxyethyl group in bacteriochlorophyll c by the hydratases BchF and BchV: adaptation of green sulfur bacteria to limited-light environments. Mol Microbiol 98:1184–1198CrossRefGoogle Scholar
  8. Harada J, Shibata Y, Teramura M, Mizoguchi T, Kinoshita Y, Yamamoto K, Tamiaki H (2018) In vivo excited energy transfer of bacteriochlorophyll c, d, e, or f to bacteriochlorophyll a in the wild-type and mutant cells of the green sulfur bacterium Chlorobaculum limnaeum. ChemPhotoChem 2:190–195CrossRefGoogle Scholar
  9. Helfrich M, Rüdiger W (1992) Various metallopheophorbides as substrates for chlorophyll synthetase. Z Naturforsc C 47:231–238CrossRefGoogle Scholar
  10. Iriyama K, Ogura N, Takamiya A (1974) A simple method for extraction and partial purification of chlorophyll from plant material, using dioxane. J Biochem 76:901–904Google Scholar
  11. Kiesel S, Wätzlich D, Lange C, Reijerse E, Bröcker MJ, Rüdiger W, Lubitz W, Scheer H, Moser J, Jahn D (2015) Iron-sulfur cluster-dependent catalysis of chlorophyllide a oxidoreductase from Roseobacter denitrificans. J Biol Chem 290:1141–1154CrossRefGoogle Scholar
  12. Kunieda M, Mizoguchi T, Tamiaki H (2004) Diastereoselective self-aggregation of synthetic 3-(1-hydroxyethyl)-bacteriopyrochlorophyll-a as a novel photosynthetic antenna model absorbing near the infrared regions. Photochem Photobiol 79:55–61CrossRefGoogle Scholar
  13. Liu Z, Bryant DA (2011) Identification of gene essential for the first committed step in the biosynthesis of bacteriochlorophyll c. J Biol Chem 286:22393–22402CrossRefGoogle Scholar
  14. Minamizaki K, Mizoguchi T, Goto T, Tamiaki H, Fujita Y (2008) Identification of two homologous genes, chlA I and chlA II, that are differentially involved in isocyclic ring formation of chlorophyll a in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 283:2684–2692CrossRefGoogle Scholar
  15. Mizoguchi T, Shoji A, Kunieda M, Miyashita H, Tsuchiya T, Mimuro M, Tamiaki H (2006) Stereochemical determination of chlorophyll-d molecule from Acaryochloris marina and its modification to a self-aggregative chlorophyll as a model of green photosynthetic bacterial antennae. Photochem Photobiol Sci 5:291–299CrossRefGoogle Scholar
  16. Mizoguchi T, Nagai C, Kunieda M, Kimura Y, Okamura A, Tamiaki H (2009) Stereochemical determination of the unique acrylate moiety at the 17-position in chlorophylls-c from a diatom Chaetoceros calcitrans and its effect upon electronic absorption properties. Org Biomol Chem 7:2120–2126CrossRefGoogle Scholar
  17. Oba T, Tamiaki H (1999) Why do chlorosomal chlorophylls lack the C132-methoxycarbonyl moiety? An in vitro model study. Photosynth Res 61:23–31CrossRefGoogle Scholar
  18. Oba T, Masada Y, Tamiaki H (1997) Convenient preparation of pheophytin b from plant extract through the C7-reduced intermediate. Bull Chem Soc Jpn 70:1905–1909CrossRefGoogle Scholar
  19. Olson JM (1998) Chlorophyll organization and function in green photosynthetic bacteria. Photochem Photobiol 67:61–75CrossRefGoogle Scholar
  20. Ouchane S, Steunou AS, Picaud M, Astier C (2004) Aerobic and anaerobic Mg-protoporphyrin monomethyl ester cyclases in purple bacteria. A strategy adopted to bypass the repressive oxygen control system. J Biol Chem 279:6385–6639CrossRefGoogle Scholar
  21. Papenbrock J, Mock HP, Tanaka R, Kruse E, Grimm B (2000) Role of magnesium chelatase activity in the early steps of the tetrapyrrole biosynthetic pathway. Plant Physiol 122:1161–1170CrossRefGoogle Scholar
  22. Tamiaki H, Kouraba M, Takeda K, Kondo S, Tanikaga R (1998) Asymmetric synthesis of methyl bacteriopheophorbide-d and analogues by stereoselective reduction of the 3-acetyl to the 3-(1-hydroxyethyl) group. Tetrahedron Asymmetry 9:2101–2111CrossRefGoogle Scholar
  23. Tamiaki H, Machida S, Mizutani K (2012) Modification of 3-substituents in (bacterio)chlorophyll derivatives to prepare 3-ethylated, methylated, and unsubstituted (nickel) pyropheophorbides and their optical properties. J Org Chem 77:4751–4758CrossRefGoogle Scholar
  24. Teramura M, Tamiaki H (2018) Semi-synthesis and HPLC analysis of (bacterio)chlorophyllides possessing a propionic acid residue at the C17-position. J Porphyrins Phthalocyanines 22:423–436CrossRefGoogle Scholar
  25. Teramura M, Harada J, Mizoguchi T, Yamamoto K, Tamiaki H (2016a) In vitro assays of BciC showing C132-demethoxycarbonylase activity requisite for biosynthesis of chlorosomal chlorophyll pigments. Plant Cell Physiol 57:1048–1052CrossRefGoogle Scholar
  26. Teramura M, Harada J, Tamiaki H (2016b) In vitro stereospecific hydration activities of the 3-vinyl group of chlorophyll derivatives by BchF and BchV enzymes involved in bacteriochlorophyll c biosynthesis of green sulfur bacteria. Photosynth Res 130:33–45CrossRefGoogle Scholar
  27. Teramura M, Harada J, Tamiaki H (2018) In vitro enzymatic assays of photosynthetic bacterial 3-vinyl hydratases for bacteriochlorophyll biosyntheses. Photosynth Res 135:319–328CrossRefGoogle Scholar
  28. Tsuchiya T, Ohta H, Okawa K, Iwamatsu A, Shimada H, Masuda T, Takamiya K (1999) Cloning of chlorophyllase, the key enzyme in chlorophyll degradation: finding of a lipase motif and the induction by methyl jasmonate. Proc Natl Acad Sci USA 96:15362–15367CrossRefGoogle Scholar
  29. Tsukatani Y, Yamamoto H, Harada J, Yoshitomi T, Nomata J, Kasahara M, Mizoguchi T, Fujita Y, Tamiaki H (2013) An unexpectedly branched biosynthetic pathway for bacteriochlorophyll b capable of absorbing near-infrared light. Sci Rep 3:1217.  https://doi.org/10.1038/srep01217 CrossRefGoogle Scholar
  30. Wakao N, Yokoi N, Isoyama N, Hiraishi A, Shimada K, Kobayashi M, Kise H, Iwaki M, Itoh S, Takaichi S (1996) Discovery of natural photosynthesis using Zn-containing bacteriochlorophyll in an aerobic bacterium Acidiphilium rubrum. Plant Cell Physiol 37:889–893CrossRefGoogle Scholar
  31. Walker JC, Willows DR (1997) Mechanism and regulation of Mg-chelatase. Biochem J 327:321–333CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Graduate School of Life SciencesRitsumeikan UniversityKusatsuJapan
  2. 2.Department of Medical BiochemistryKurume University School of MedicineKurumeJapan

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