Advertisement

Spectral signatures of five hydroxymethyl chlorophyll a derivatives chemically derived from chlorophyll b or chlorophyll f

  • Artur Sawicki
  • Robert D. Willows
  • Min Chen
Original Article
  • 76 Downloads

Abstract

Chlorophylls (Chls) are pigments involved in light capture and light reactions in photosynthesis. Chl a, Chl b, Chl d, and Chl f are characterized by unique absorbance maxima in the blue (Soret) and red (Qy) regions with Chl b, Chl d, and Chl f each possessing a single formyl group at a unique position. Relative to Chl a the Qy absorbance maximum of Chl b is blue-shifted while Chl d and Chl f are red-shifted with the shifts attributable to the relative positions of the formyl substitutions. Reduction of a formyl group of Chl b to form 7-hydroxymethyl Chl a, or oxidation of the vinyl group of Chl a into a formyl group to form Chl d was achieved using sodium borohydride (NaBH4) or β-mercaptoethanol (BME/O2), respectively. During the consecutive reactions of Chl b and Chl f using a three-step procedure (1. NaBH4, 2. BME/O2, and 3. NaBH4) two new 7-hydroxymethyl Chl a species were prepared possessing the 3-formyl or 3-hydroxymethyl groups and three new 2-hydroxymethyl Chl a species possessing the 3-vinyl, 3-formyl, or 3-hydroxymethyl groups, respectively. Identification of the spectral properties of 2-hydroxymethyl Chl a may be biologically significant for deducing the latter stages of Chl f biosynthesis if the mechanism parallels Chl b biosynthesis. The spectral features and chromatographic properties of these modified Chls are important for identifying potential intermediates in the biosynthesis of Chls such as Chl f and Chl d and for identification of any new Chls in nature.

Keywords

Chlorophyll Chlorophyll derivative Chlorophyll f Vinyl oxidation Hydroxymethyl Formyl reduction 

Abbreviations

BME

β-Mercaptoethanol

CAO

Chlorophyll a oxygenase

CBR

Chlorophyll b reductase

Chl

Chlorophyll

Chlide

Chlorophyllide

HCAR

Hydroxymethyl-chlorophyll a reductase

MALDI-MS

Matrix-assisted laser desorption/ionization mass spectrometry

NaBH4

Sodium borohydride

RP-HPLC

Reversed-phase high-performance liquid chromatography

Notes

Acknowledgements

We would like to thank Dr. Ben Crossett for access to the mass spectrometry facility at the Charles Perkins Centre, The University of Sydney. We also thank Dr. Ann Kwan for assisting with the NMR experiments.

Funding

The research is supported by The Australian Research Council Centre of Excellence for Translational Photosynthesis (CE20140100015).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human or animal subjects performed by any of the authors.

Supplementary material

11120_2018_611_MOESM1_ESM.pdf (854 kb)
Supplementary material 1 (PDF 853 KB)

References

  1. Björn LO, Papageorgiou GC, Blankenship RE, Govindjee (2009) A viewpoint: why chlorophyll a? Photosynth Res 99(2):85–98.  https://doi.org/10.1007/s11120-008-9395-x CrossRefGoogle Scholar
  2. Borch RF, Bernstein MD, Durst HD (1971) Cyanohydridoborate anion as a selective reducing agent. J Am Chem Soc 93(12):2897–2904.  https://doi.org/10.1021/ja00741a013 CrossRefGoogle Scholar
  3. Chaikin SW, Brown WG (1949) Reduction of aldehydes, ketones and acid chlorides by sodium borohydride. J Am Chem Soc 71(1):122–125.  https://doi.org/10.1021/ja01169a033 CrossRefGoogle Scholar
  4. Chen M (2014) Chlorophyll modifications and their spectral extension in oxygenic photosynthesis. Annu Rev Biochem 83(1):317–340.  https://doi.org/10.1146/annurev-biochem-072711-162943 doiCrossRefGoogle Scholar
  5. Chen M, Schliep M, Willows RD, Cai Z-L, Neilan BA, Scheer H (2010) A red-shifted chlorophyll. Science 329(5997):1318–1319.  https://doi.org/10.1126/science.1191127 CrossRefGoogle Scholar
  6. Chen M, Li Y, Birch D, Willows RD (2012) A cyanobacterium that contains chlorophyll f—a red-absorbing photopigment. FEBS Lett 586(19):3249–3254.  https://doi.org/10.1016/j.febslet.2012.06.045 CrossRefGoogle Scholar
  7. Eggink LL, Park H, Hoober JK (2001) The role of chlorophyll b in photosynthesis: hypothesis. BMC Plant Biol 1(1):2.  https://doi.org/10.1186/1471-2229-1-2 CrossRefGoogle Scholar
  8. Eggink LL, LoBrutto R, Brune DC, Brusslan J, Yamasato A, Tanaka A, Hoober JK (2004) Synthesis of chlorophyll b: localization of chlorophyllide a oxygenase and discovery of a stable radical in the catalytic subunit. BMC Plant Biol 4:5.  https://doi.org/10.1186/1471-2229-4-5 CrossRefGoogle Scholar
  9. Fukusumi T, Matsuda K, Mizoguchi T, Miyatake T, Ito S, Ikeda T, Tamiaki H, Oba T (2012) Non-enzymatic conversion of chlorophyll-a into chlorophyll-d in vitro: a model oxidation pathway for chlorophyll-d biosynthesis. FEBS Lett 586(16):2338–2341.  https://doi.org/10.1016/j.febslet.2012.05.036 CrossRefGoogle Scholar
  10. Garg H, Loughlin PC, Willows RD, Chen M (2017) The C21-formyl group in chlorophyll f originates from molecular oxygen. J Biol Chem 292(47):19279–19289.  https://doi.org/10.1074/jbc.M117.814756 CrossRefGoogle Scholar
  11. Gouterman M, Wagnière GH, Snyder LC (1963) Spectra of porphyrins: Part II. Four orbital model. J Mol Spectrosc 11(1):108–127.  https://doi.org/10.1016/0022-2852(63)90011-0 CrossRefGoogle Scholar
  12. Ho M-Y, Shen G, Canniffe DP, Zhao C, Bryant DA (2016) Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II. Science 353 (6302).  https://doi.org/10.1126/science.aaf9178
  13. Hohmann-Marriott MF, Blankenship RE (2011) Evolution of photosynthesis. Annu Rev Plant Biol 62(1):515–548.  https://doi.org/10.1146/annurev-arplant-042110-103811 CrossRefGoogle Scholar
  14. Holt AS (1959) Reduction of chlorophyllides, chlorophylls and chlorophyll derivatives by sodium borohydride. Plant Physiol 34(3):310–314CrossRefGoogle Scholar
  15. Holt AS, Morley HV (1959) A proposed structure for chlorophyll d. Can J Chem 37(3):507–514.  https://doi.org/10.1139/v59-069 CrossRefGoogle Scholar
  16. Hoober JK, Eggink LL, Chen M (2007) Chlorophylls, ligands and assembly of light-harvesting complexes in chloroplasts. Photosynth Res 94(2):387–400.  https://doi.org/10.1007/s11120-007-9181-1 CrossRefGoogle Scholar
  17. Hu Q, Miyashita H, Iwasaki I, Kurano N, Miyachi S, Iwaki M, Itoh S (1998) A photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis. Proc Natl Acad Sci USA 95(22):13319–13323.  https://doi.org/10.1073/pnas.95.22.13319 CrossRefGoogle Scholar
  18. Hynninen PH, Kaartinen V, Kolehmainen E (2010) Horseradish peroxidase-catalyzed oxidation of chlorophyll a with hydrogen peroxide: characterization of the products and mechanism of the reaction. Biochim Biophys Acta 1797(5):531–542.  https://doi.org/10.1016/j.bbabio.2010.01.017 CrossRefGoogle Scholar
  19. Hynninen Paavo H, Sievers G (1981) Conformations of chlorophylls a and a′ and their magnesium-free derivatives as revealed by circular dichroism and proton magnetic resonance. znb 36 (8):1000–1009.  https://doi.org/10.1515/znb-1981-0819
  20. Hyvärinen K, Helaja J, Kuronen P, Kilpeläinen I, Hynninen PH (1995)) 1H and 13C NMR spectra of the methanolic allomerization products of 132(R)-chlorophyll a. Magn Reson Chem 33(8):646–656.  https://doi.org/10.1002/mrc.1260330806 doiCrossRefGoogle Scholar
  21. Ito H, Ohtsuka T, Tanaka A (1996) Conversion of chlorophyll b to chlorophyll a via 7-hydroxymethyl chlorophyll. J Biol Chem 271(3):1475–1479.  https://doi.org/10.1074/jbc.271.3.1475 CrossRefGoogle Scholar
  22. Keller MD, Selvin RC, Claus W, Guillard RRL (1987) Media for the culture of oceanic ultraphytoplankton. J Phycol 23(4):633–638.  https://doi.org/10.1111/j.1529-8817.1987.tb04217.x doiCrossRefGoogle Scholar
  23. Koizumi H, Itoh Y, Hosoda S, Akiyama M, Hoshino T, Shiraiwa Y, Kobayashi M (2005) Serendipitous discovery of Chl d formation from Chl a with papain. Sci Technol Adv Mater 6(6):551–557.  https://doi.org/10.1016/j.stam.2005.06.022 CrossRefGoogle Scholar
  24. Kräutler B (2011) A new factor in life’s quest for energy. Angew Chem Int Ed Engl 50(11):2439–2441.  https://doi.org/10.1002/anie.201007339 doiCrossRefGoogle Scholar
  25. Kume A, Akitsu T, Nasahara KN (2018) Why is chlorophyll b only used in light-harvesting systems? J Plant Res.  https://doi.org/10.1007/s10265-018-1052-7 Google Scholar
  26. Kusunoki M, Tamiaki H (2018) Synthesis of 7-substituted chlorophyll-a derivatives as chlorophyll-b analogs with specific visible absorption bands. Tetrahedron 74(4):453–464.  https://doi.org/10.1016/j.tet.2017.12.013 CrossRefGoogle Scholar
  27. Lane CF (1975) Sodium cyanoborohydride—a highly selective reducing agent for organic functional groups. Synthesis 1975 (03):135–146.  https://doi.org/10.1055/s-1975-23685
  28. Li Y, Lin Y, Loughlin P, Chen M (2014) Optimization and effects of different culture conditions on growth of Halomicronema hongdechloris—a filamentous cyanobacterium containing chlorophyll f. Front Plant Sci 5 (67).  https://doi.org/10.3389/fpls.2014.00067
  29. Li Y, Vella N, Chen M (2018) Characterization of isolated photosystem I from Halomicronema hongdechloris, a chlorophyll f-producing cyanobacterium. Photosynthetica 56(1):306–315.  https://doi.org/10.1007/s11099-018-0776-x CrossRefGoogle Scholar
  30. Loughlin PC, Willows RD, Chen M (2014) In vitro conversion of vinyl to formyl groups in naturally occurring chlorophylls. Sci Rep 4:6069.  https://doi.org/10.1038/srep06069 CrossRefGoogle Scholar
  31. Loughlin PC, Willows RD, Min C (2015) Hydroxylation of the C132 and C18 carbons of chlorophylls by heme and molecular oxygen. J Porphyr Phthalocyanines 19(09):1007–1013.  https://doi.org/10.1142/s1088424615500571 CrossRefGoogle Scholar
  32. Manning WM, Strain HH (1943) Chlorophyll d, a green pigment of red algae. J Biol Chem 151(1):1–19Google Scholar
  33. Meguro M, Ito H, Takabayashi A, Tanaka R, Tanaka A (2011) Identification of the 7-hydroxymethyl chlorophyll a reductase of the chlorophyll cycle in Arabidopsis. Plant Cell 23(9):3442–3453.  https://doi.org/10.1105/tpc.111.089714 CrossRefGoogle Scholar
  34. Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M, Miyachi S (1996) Chlorophyll d as a major pigment. Nature 383:402.  https://doi.org/10.1038/383402a0 CrossRefGoogle Scholar
  35. Nürnberg DJ, Morton J, Santabarbara S, Telfer A, Joliot P, Antonaru LA, Ruban AV, Cardona T, Krausz E, Boussac A, Fantuzzi A, Rutherford AW (2018) Photochemistry beyond the red limit in chlorophyll f-containing photosystems. Science 360(6394):1210–1213.  https://doi.org/10.1126/science.aar8313 CrossRefGoogle Scholar
  36. Oba T, Uda Y, Matsuda K, Fukusumi T, Ito S, Hiratani K, Tamiaki H (2011) A mild conversion from 3-vinyl- to 3-formyl-chlorophyll derivatives. Bioorg Med Chem Lett 21(8):2489–2491.  https://doi.org/10.1016/j.bmcl.2011.02.054 CrossRefGoogle Scholar
  37. Oster U, Tanaka R, Tanaka A, 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(3):305–310.  https://doi.org/10.1046/j.1365-313x.2000.00672.x doiCrossRefGoogle Scholar
  38. Partensky F, Six C, Ratin M, Garczarek L, Vaulot D, Probert I, Calteau A, Gourvil P, Marie D, Grébert T, Bouchier C, Le Panse S, Gachenot M, Rodríguez F, Garrido JL (2018) A novel species of the marine cyanobacterium Acaryochloris with a unique pigment content and lifestyle. Sci Rep 8(1):9142.  https://doi.org/10.1038/s41598-018-27542-7 CrossRefGoogle Scholar
  39. Reinbothe S, Pollmann S, Reinbothe C (2003) In situ conversion of protochlorophyllide b to protochlorophyllide a in barley: evidence for a novel role of 7-formyl reductase in the prolamellar body of etioplasts. J Biol Chem 278(2):800–806.  https://doi.org/10.1074/jbc.M209737200 CrossRefGoogle Scholar
  40. Scheumann V, Schoch S, Rüdiger W (1998) Chlorophyll a formation in the chlorophyll b reductase reaction requires reduced ferredoxin. J Biol Chem 273(52):35102–35108.  https://doi.org/10.1074/jbc.273.52.35102 CrossRefGoogle Scholar
  41. Schliep M, Crossett B, Willows RD, Chen M (2010)) 18O labeling of chlorophyll d in Acaryochloris marina reveals that chlorophyll a and molecular oxygen are precursors. J Biol Chem 285(37):28450–28456.  https://doi.org/10.1074/jbc.M110.146753 CrossRefGoogle Scholar
  42. Schmitt F-J, Campbell ZY, Bui MV, Hüls A, Tomo T, Chen M, Maksimov EG, Allakhverdiev SI, Friedrich T (2018) Photosynthesis supported by a chlorophyll f-dependent, entropy-driven uphill energy transfer in Halomicronema hongdechloris cells adapted to far-red light. Photosynth Res.  https://doi.org/10.1007/s11120-018-0556-2 Google Scholar
  43. Strain HH, Manning WM (1942) Isomerization of chlorophylls a and b. J Biol Chem 146(1):275–276Google Scholar
  44. Tamiaki H, Miyata S, Kureishi Y, Tanikaga R (1996) Aggregation of synthetic zinc chlorins with several esterified alkyl chains as models of bacteriochlorophyll-c homologs. Tetrahedron 52(38):12421–12432.  https://doi.org/10.1016/0040-4020(96)00740-5 CrossRefGoogle Scholar
  45. Tanaka A, Ito H, Tanaka R, Tanaka NK, Yoshida K, Okada K (1998) Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc Natl Acad Sci 95(21):12719–12723CrossRefGoogle Scholar
  46. Tomo T, Suzuki T, Hirano E, Tsuchiya T, Miyashita H, Dohmae N, Mimuro M (2006) Reversible absorption change of chlorophyll d in solutions. Chem Phys Lett 423(4):282–287.  https://doi.org/10.1016/j.cplett.2006.03.091 CrossRefGoogle Scholar
  47. Tsuchiya T, Mizoguchi T, Akimoto S, Tomo T, Tamiaki H, Mimuro M (2012) 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 Cell Physiol 53(3):518–527.  https://doi.org/10.1093/pcp/pcs007 CrossRefGoogle Scholar
  48. Voitsekhovskaja OV, Tyutereva EV (2015) Chlorophyll b in angiosperms: functions in photosynthesis, signaling and ontogenetic regulation. J Plant Physiol 189:51–64.  https://doi.org/10.1016/j.jplph.2015.09.013 CrossRefGoogle Scholar
  49. Xu M, Kinoshita Y, Tamiaki H (2014) Synthesis of chlorophyll-f analogs possessing the 2-formyl group by modifying chlorophyll-a. Bioorg Med Chem Lett 24(16):3997–4000.  https://doi.org/10.1016/j.bmcl.2014.06.022 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.School of Life and Environmental SciencesUniversity of SydneySydneyAustralia
  2. 2.Department of Molecular SciencesMacquarie UniversitySydneyAustralia

Personalised recommendations