Skip to main content
SpringerLink
Log in

Chromatic photoacclimation extends utilisable photosynthetically active radiation in the chlorophyll d-containing cyanobacterium, Acaryochloris marina

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Chromatic photoacclimation and photosynthesis were examined in two strains of Acaryochloris marina (MBIC11017 and CCMEE5410) and in Synechococcus PCC7942. Acaryochloris contains Chl d, which has an absorption peak at ca 710 nm in vivo. Cultures were grown in one of the three wavelengths (525 nm, 625 nm and 720 nm) of light from narrow-band photodiodes to determine the effects on pigment composition, growth rate and photosynthesis: no growth occurred in 525 nm light. Synechococcus did not grow in 720 nm light because Chl a does not absorb effectively at this long wavelength. Acaryochloris did grow in 720 nm light, although strain MBIC11017 showed a decrease in phycobilins over time. Both Synechococcus and Acaryochloris MBIC11017 showed a dramatic increase in phycobilin content when grown in 625 nm light. Acaryochloris CCMEE5410, which lacks phycobilins, would not grow satisfactorily under 625 nm light. The cells adjusted their pigment composition in response to the light spectral conditions under which they were grown. Photoacclimation and the Q y peak of Chl d could be understood in terms of the ecological niche of Acaryochloris, i.e. habitats enriched in near infrared radiation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

Chl:

Chlorophyll

LED:

Light emitting diode

NIR:

The near infrared light

PAR:

Photosynthetically active radiation

PBS:

Phycobilisomes

PS:

Photosystem

References

  • Björn LO, Papageorgiou GC, Blankenshp RE, Govindjee (2009) A viewpoint: why chlorophyll a? Photosynth Res 99:85–98

    Article  PubMed  CAS  Google Scholar 

  • Blankenship RE (2002) Molecular mechanisms of photosynthesis. Blackwell, Oxford, UK

    Book  Google Scholar 

  • Boulay C, Abasova L, Six C, Vass I, Kirilovsky D (2008) Occurrence and function of the orange carotenoid protein in photoprotective mechanisms in various cyanobacteria. Biochim Biophys Acta. 1777:1344–1354

    Article  PubMed  CAS  Google Scholar 

  • Chan YW, Nenninger A, Clokie SJH, Mann NH, Scanlan DJ, Whitworth AL, Clokie MRJ (2007) Pigment composition and adaptation in free-living and symbiotic strains of Acaryochloris marina. FEMS Microbiol Ecol 61:65–73

    Article  PubMed  CAS  Google Scholar 

  • Chen M, Quinnell RG, Larkum AWD (2002) Chlorophyll d as the major photopigment in Acaryochloris marina. J Porphyrins Phthalocyanines 6:763–773

    Article  CAS  Google Scholar 

  • Cinque G, Croce R, Bassi R (2000) Absorption spectra of chlorophyll a and b in Lhcb protein environment. Photosynth Res 64:233–242

    Article  PubMed  CAS  Google Scholar 

  • Croce R, Cinque G, Holzwarth AR, Bassi R (2000) The Soret absorption properties of carotenoids and chlorophylls in antenna complexes of higher plants. Photosynth Res 64:221–231

    Article  PubMed  CAS  Google Scholar 

  • Falkowski PG, Laroche J (1991) Acclimation to spectral irradiance in algae. J Phycol 27:8–14

    Article  Google Scholar 

  • French CS, Brown JS, Lawrence MC (1972) Four universal forms of chlorophyll a. Plant Physiol 49:421–429

    Article  PubMed  CAS  Google Scholar 

  • Gloag RS, Ritchie RJ, Chen M, Larkum AWD, Quinnell RG (2007) Chromatic photoacclimation, photosynthetic electron transport and oxygen evolution in the chlorophyll d-containing oxyphotobacterium Acaryochloris marina. Biochim Biophys Acta-Bioenergetics 1767:127–135

    Article  CAS  Google Scholar 

  • Gobets B, van Grondelle R (2001) Energy transfer and trapping in photosystem I. Biochim Biophys Acta 1507:80–99

    Article  PubMed  CAS  Google Scholar 

  • Grossman AR (2003) A molecular understanding of complementary chromatic adaptation. Photosynth Res 76:207–215

    Article  PubMed  CAS  Google Scholar 

  • Haardt H, Maske H (1987) Specific in vivo absorption-coefficient of chlorophyll a at 675 nm. Limnol Oceanogr 32:608–619

    Article  CAS  Google Scholar 

  • Holt AS, Morley HV (1959) A proposed structure for chlorophyll d. Can J Chem 37:507–514

    Article  CAS  Google Scholar 

  • Hu Q, Marquardt J, Iwasaki I, Miyashita H, Kurano N, Mörschel E, Miyachi S (1999) Molecular structure, localization and function of biliproteins in the chlorophyll a/d containing oxygenic photosynthetic prokaryote Acaryochloris marina. Biochim Biophys Acta-Bioenergetics 1412:250–261

    Article  CAS  Google Scholar 

  • Jeffrey SW, Vesk M (1997) Introduction to marine phytoplankton and their pigment signatures. In: Jeffrey SW, Mantoura RFC, Wright SW (eds) Phytoplankton Pigments in Oceanography: Guidelines to Modern Methods. UNESCO Publ, Paris, pp 37–84

    Google Scholar 

  • Kashiyama Y, Miyashita H, Ohkubo S, Ogawa NO, Chikaraishi Y, Takano Y, Suga H, Toyofuku T, Nomaki H, Kitazato H, Nagata T, Ohkouchi N (2008) Evidence of global Chlorophyll d. Science 321:658

    Article  PubMed  CAS  Google Scholar 

  • Kehoe DM, Gutu A (2006) Responding to color: the regulation of complementary chromatic adaptation. Ann Rev Plant Biol 57:127–150

    Article  CAS  Google Scholar 

  • Kiang NY, Siefert J, Govindjee, Blankenship RE (2007) Spectral signatures of photosynthesis I. Rev Earth org Astrobiol 7:222–251

    Article  CAS  Google Scholar 

  • Kirilovsky D (2007) Photoprotection in cyanobacteria: the orange carotenoid protein (OCP)-related non-photochemical-quenching mechanism. Photosynth Res 93:7–16

    Article  PubMed  CAS  Google Scholar 

  • Knapp EW, Fischer SF, Zinth W, Sander M, Kaiser W, Deisenhofer J, Michel H (1985) Analysis of optical-spectra from single-crystals of Rhodopseudomonas viridis reaction centers. Proc Natl Acad Sci USA 82:8463–8467

    Article  PubMed  CAS  Google Scholar 

  • Kühl M, Larkum AWD (2001) The microenvironment and photosynthetic performance of Prochloron sp in symbiosis with didemnid ascidians. In: Seckbach J (ed) Symbiosis. Kluwer, Dordrecht, pp 273–290

  • Kühl M, Chen M, Ralph PJ, Schreiber U, Larkum AWD (2005) A niche for cyanobacteria containing chlorophyll d. Nature 433:820

    Article  PubMed  CAS  Google Scholar 

  • Kühl M, Chen M, Larkum AWD (2007) Biology of the chlorophyll d-containing cyanobacterium Acaryochloris marina. In: Seckbach J (ed) Algae and cyanobacteria in extreme environments. Springer, Berlin, pp 101–123

    Chapter  Google Scholar 

  • Lapouge K, Naveke A, Gall A, Ivancich A, Seguin J, Scheer H, Sturgis JN, Mattioli TA, Robert B (1999) Conformation of bacteriochlorophyll molecules in photosynthetic proteins from purple bacteria. Biochem 38:11115–11121

    Article  CAS  Google Scholar 

  • Larkum AWD, Kühl M (2005) Chlorophyll d: the puzzle resolved. Trends Plant Sci 10:355–357

    Article  PubMed  CAS  Google Scholar 

  • MacIntyre HL, Kana TM, Anning T, Geider RJ (2002) Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J Phycol 38:17–38

    Article  Google Scholar 

  • Manning WM, Strain HH (1943) Chlorophyll d, a green pigment of red algae. J Biol Chem 151:1–19

    CAS  Google Scholar 

  • Marquardt J, Senger H, Miyashita H, Miyachi S, Morschel E (1997) Isolation and characterization of biliprotein aggregates from Acaryochloris marina, a Prochloron-like prokaryote containing mainly chlorophyll d. FEBS Lett 410:428–432

    Article  PubMed  CAS  Google Scholar 

  • Miller SR, Augustine S, Olson TL, Blankenship RE, Selker J, Wood AM (2005) Discovery of a free-living chlorophyll d-producing cyanobacterium with a hybrid proteobacterial/cyanobactyerial small-subunit rRNA gene. Proc Natl Acad Sci USA 102:850–855

    Article  PubMed  CAS  Google Scholar 

  • Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M, Miyachi S (1996) Chlorophyll d as a major pigment. Nature 383:402

    Article  CAS  Google Scholar 

  • Miyashita H, Adachi K, Kurano N, Ikemoto H, Chihara M, Miyachi S (1997) Pigment composition of a novel oxygenic photosynthetic prokaryote containing chlorophyll d as the major chlorophyll. Plant Cell Physiol 38:274–281

    CAS  Google Scholar 

  • Miyashita H, Ikemoto H, Kurano N, Miyachi S, 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

    Article  CAS  Google Scholar 

  • Montgomery BL (2008) Shedding new light on the regulation of complementary chromatic adaptation. Cent Eur J Biol 3(4):351–358

    Article  CAS  Google Scholar 

  • Moore LR, Goericke R, Chisholm SW (1995) Comparative physiology of Synechococcus and Prochlorococcus - Influence of light and temperature on growth, pigments, fluorescence and absorptive properties. Marine Ecol Prog Ser 116:259–275

    Article  Google Scholar 

  • Mullineaux CW (2001) How do cyanobacteria sense and respond to light? Mol Microbiol 41:965–971

    Article  PubMed  CAS  Google Scholar 

  • Murakami A, Miyashita H, Iseki M, Adachi K, Mimuro M (2004) Chlorophyll d in an epiphytic cyanobacterium of red algae. Science 303:1633

    Article  PubMed  CAS  Google Scholar 

  • Nieuwenburg P, Clarke RJ, Cai Z-L, Chen M, Larkum AWD, Cabral NM, Ghiggino KP, Reimers JR (2003) Examination of the photophysical processes of chlorophyll d leading to a clarification of proposed uphill energy transfer processes in cells of Acaryochloris marina. Photochem Photobiol 77:628–637

    Article  PubMed  CAS  Google Scholar 

  • Ohkubo S, Miyashita H, Murakami A, Takeyama H, Tsuchiya T, Mimuro M (2006) Molecular detection of epiphytic Acaryochloris spp. on marine macroalgae. Appl Environ Microbiol 72:7912–7915

    Article  PubMed  CAS  Google Scholar 

  • Palenik B (2001) Chromatic adaptation in marine Synechococcus strains. App Environ Microbiol 67:991–994

    Article  CAS  Google Scholar 

  • Perry MJ, Talbot MC, Alberte RS (1981) Photoadaptation in marine-phytoplankton: response of the photosynthetic unit. Marine Biol 62:91–101

    Article  CAS  Google Scholar 

  • Petrášek Z, Schmitt FJ, Theiss C, Huyer J, Chen M, Larkum A, Eichler HJ, Kemnitz K, Eckert HJ (2005) Excitation energy transfer from phycobiliprotein to chlorophyll d in intact cells of Acaryochloris marina studied by time- and wavelength resolved fluorescence spectroscopy. Photochem Photobiol Sci 4:1016–1022

    Article  PubMed  CAS  Google Scholar 

  • Rippka RJ, Waterbury B, Stanier RY (1981) Isolation and purification of cyanobacteria: some general principles. J General Microbiol 111:1–161

    Google Scholar 

  • Ritchie RJ (2006) Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth Res 89:27–41

    Article  PubMed  CAS  Google Scholar 

  • Ritchie RJ (2008) Universal chlorophyll equations for estimating chlorophylls a, b, c & d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol or ethanol solvents. Photosynthetica 46:115–126

    Article  CAS  Google Scholar 

  • Scheer H (ed) (1991) Chlorophylls. CRC Press, Boca Raton, USA

  • Scott M, McCollum C, Vasilev S, Crozier C, Espie GS, Krol M, Huner NPA, Bruce D (2006) Mechanism of the down regulation of photosynthesis by blue light in the cyanobacterium Synechocystis sp. Biochem 45:8952–8958

    Article  CAS  Google Scholar 

  • Six C, Thomas J-C, Thion L, Lemoine Y, Zal F, Partensky F (2005) Two novel phycoerythrin-associated linker proteins in the marine cyanobacterium Synechococcus sp. strain WH8102. J Bacteriol 187:1685–1694

    Article  PubMed  CAS  Google Scholar 

  • Stanier RY, Bazine GC (1977) Phototrophic prokaryotes: the cyanobacteria. Ann Rev Microbiol 31:225–274

    Article  CAS  Google Scholar 

  • Stomp M, Huisman J, de Jongh F, Veraart AJ, Gerla D, Rijkeboer M, Ibelings BW, Wollenzien UIA, Stal LJ (2004) Adaptive divergence in pigment composition promotes phytoplankton biodiversity. Nature 432:104–107

    Article  PubMed  CAS  Google Scholar 

  • Swingley WD, Chen M, Cheung PC, Conrad AL, Dejesa LC, Hao J, Honchak BM, Karbach LE, Kurdoglu A, Lahiri S, Mastrian SD, Miyashita H, Page L, Ramakrishna P, Satoh S, Sattley WM, Shimada Y, Taylor HL, Tomo T, Tsuchiya T, Wang ZT, Raymond J, Mimuro M, Blankenship RE, Touchman JW (2008) Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina. Proc Natl Acad Sci USA 105:2005–2010

    Article  PubMed  CAS  Google Scholar 

  • Wilson A, Ajlani G, Verbavatz JM, Vass I, Kerfeld CA (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18:992–1007

    Article  PubMed  CAS  Google Scholar 

  • Wu YP, Krogmann DW (1997) The orange carotenoid protein of Synechocystis PCC 6803. Biochim Biophys Acta 1322:1–7

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgement

MC holds an Australian Research Council (ARC) QEII fellow and wishes to thank ARC for the financial support.

Author information

Authors and Affiliations

  1. School of Biological Sciences (A08), University of Sydney, Sydney, NSW, 2006, Australia

    Zane Duxbury, Martin Schliep, Raymond J. Ritchie, Anthony W. D. Larkum & Min Chen

Authors
  1. Zane Duxbury
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martin Schliep
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Raymond J. Ritchie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anthony W. D. Larkum
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Min Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Min Chen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

11120_2009_9466_MOESM1_ESM.jpg

Figure supplementary 1. Growth rate. Growing rate was determined by monitoring the A708 absorbance (Chl d Q y peak) and the fitting curve was modelled using an exponential curve equation (as in the figure). Grey dashed line, CCMEE5410 grown in 720 nm light; Black dashed line, MBIC11017 grown in 720 nm light; Black solid line, Acaryochloris MBIC11017 grown in 625 nm light and grey solid line, Acaryochloris CCMEE5410 grown in 625 nm. (JPG 326 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Duxbury, Z., Schliep, M., Ritchie, R.J. et al. Chromatic photoacclimation extends utilisable photosynthetically active radiation in the chlorophyll d-containing cyanobacterium, Acaryochloris marina . Photosynth Res 101, 69–75 (2009). https://doi.org/10.1007/s11120-009-9466-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-009-9466-7

Keywords

Search

Navigation