Skip to main content
Log in

A new type of complementary chromatic adaptation exemplified byPhormidium sp. C86: Changes in the number of peripheral rods and in the stoichiometry of core complexes in phycobilisomes

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

The marine cyanobacteriumPhormidium sp. strain C86 changes the phycobilisome type depending on light quality. Red-light-adapted cells contained hemidiscoidal phycobilisomes with a photosystem II:phycobilisome ratio of 2.2, while green-light-adapted cells exhibited hemiellipsoidal phycobilisomes with a photosystem II:phycobilisome ratio of 4.4, as determined by a combined analysis of freeze-fractured thylakoid membranes and ultrathin sections and by photochemical determinations of photosystems and phycobilisomes. Core complexes of phycobilisomes of red- and green-light-adapted cells were isolated by affinity chromatography and were subsequently separated into two allophycocyanin-containing fractions. The high-molecular-weight fraction, with a sedimentation coefficient of 24 S and a calculated mol. wt. of 860,000, contained complexes of the quaternary structure (α AP9 β AP8 β19.5AP)2·(LCM)2 and tricylindrical shape, previously designated APCM. This fraction was similar in size in red- and green-light-adapted cells; however, differences were detected in the low-molecular-weight allophycocyanin fraction containing the “trimeric” complexes with a sedimentation coefficient of 6 S. As shown by comparison of spectral and stoichiometric data of intact phycobilisomes and isolated core complexes, the amount of the αAPB-containing core complex (α AP2 αAPBβ AP3 ·L 10C ) was greater in core fractions of green-light phycobilisomes, whereas the amount of the core complexes (α AP3 β AP3 ·L 10C ) designated AP·L 10C , was higher in cores of red-light phycobilisomes.Phormidium sp. is the first organism examined that exhibits a new type of complementary chromatic adaptation by altering the composition of the phycobilisome core and the number and composition of peripheral rods and by changing the ratio of photosystem II to phycobilisomes. A model summarizing the structural consequences of the results is presented.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

AP :

“Trimeric” allophycocyanin complex of the structure (α AP3 β AP3 )

APB :

“Trimeric” αAPB containing allophycocyanin complex of the structure (α AP2 αAPBβ AP3 )

AP CM :

Allophycocyanin core membrane complex of the structure (α AP9 β AP8 β19.5AP)

AP·L 10C :

“Trimeric” allophycocyanin complex of the structure (α AP3 β AP3 )·L 10C

Chl :

Chlorophyll

EF :

Exoplasmic fracture face

GL :

Green light

L C :

Phycobilisome core linker polypeptide

L CM :

Phycobilisome core-membrane linker polypeptide

P700 :

Reaction center of photosystem I

PBS :

Phycobilisome

PC :

Phycocyanin

PE :

Phycoerythrin

PF :

Protoplasmic fracture face

PMSF :

Phenylmethanesulfonylfluoride

PS I :

Photosystem I

PS II :

Photosystem II

RL :

Red light

S :

Sedimentation coefficient

References

  • Anderson LK, Eiserling FA (1986) Asymmetrical core structure in phycobilisomes of the cyanobacteriumSynechocystis 6701. J Mol Biol 191:441–451

    Article  PubMed  CAS  Google Scholar 

  • Bennett A, Bogorad L (1973) Complementary chromatic adaptation in a filamentous blue-green alga. J Cell Biol 58:419–435

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilising the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Bryant DA (1988) Genetic analysis of phycobilisome biosynthesis, assembly, structure, and function in the cyanobacteriumSynechococcus sp. PCC 7002. In: Stevens SE Jr, Bryant DA (eds) Light-energy transduction in photosynthesis: higher plant and bacterial models, American Society of Photobiologists, Rockville, pp 62–90

    Google Scholar 

  • Bryant DA (1991) Cyanobacterial phycobilisomes: progress toward complete structural and functional analysis via molecular genetics. In: Bogorad L, Vasil IK (eds) Cell culture and somatic cell genetics of plants, vol 7B. Academic Press, New York, pp 257–300

    Google Scholar 

  • Bryant DA, Guglielmi G, Tandeau de Marsac N, Castets AM, Cohen-Bazire G (1979) The structure of cyanobacterial phycobilisomes: a model. Arch Microbiol 123:113–127

    Article  CAS  Google Scholar 

  • Capuano V, Braux AS, Tandeau de Marsac N, Houmard J (1991) The “anchor polypeptide” of cyanobacterial phycobilisomes. Molecular characterization of theSynechococcus sp. PCC 6301apcE gene. J Biol Chem 266:7239–7247

    PubMed  CAS  Google Scholar 

  • Clement-Metral JD, Gantt E, Redlinger T (1985) A photosystem II-phycobilisome preparation from the red algaePorphyridium cruentum: oxygen evolution, ultrastructure and polypeptide resolution. Arch Biochem Biophys 238:10–17

    Article  PubMed  CAS  Google Scholar 

  • Cunningham FX, Dennenberg RJ, Jursinic PA, Gantt E (1990) Growth under red light enhances photosystem II relative to photosystem I and phycobilisomes in the red algaPorphyridium cruentum Plant Physiol 93:888–895

    PubMed  CAS  Google Scholar 

  • Gantt E (1981) Phycobilisomes. Annu Rev Plant Physiol 32:327–347

    Article  CAS  Google Scholar 

  • Giddings TH, Wasmann C, Staehelin LA (1983) Structure of the thylakoids and envelope membranes of the cyanelles ofCyanophora paradoxa Plant Physiol 71:409–419

    PubMed  CAS  Google Scholar 

  • Gindt YM, Zhou J, Bryant DA, Glazer AN, Sauer K (1992) Core mutations ofSynechococcus sp. PCC 7002 phycobilisomes: a spectroscopic study. J Photochem Photobiol B 15:75–89

    Article  PubMed  CAS  Google Scholar 

  • Glazer AN (1985) Light harvesting by phycobilisomes. Annu Rev Biophys Biophys Chem 14:47–77

    Article  PubMed  CAS  Google Scholar 

  • Glazer AN, Chan C, Yeh SW, Clark JH (1985) Kinetics of energy flow in the phycobilisome core. Science 230:1051–1053

    Article  CAS  PubMed  Google Scholar 

  • Grossman AR, Lemaux PG, Conley PB, Burns BU, Anderson LK (1988) Characterization of phycobiliprotein genes inFremyella diplosiphon and their regulated expression during complementary chromatic adaptation. Photosynthesis Res 17:23–56

    Article  CAS  Google Scholar 

  • Hiyama T, Ke B (1972) Difference spectra and extinction coefficients of P700. Biochim Biophys Acta 267:160–171

    Article  PubMed  CAS  Google Scholar 

  • Holzwarth AR, Bittersmann E, Reuter W, Wehrmeyer W (1990) Studies on chromophore coupling in isolated phycobiliproteins. 3. Picosecond excited state kinetics and time-resolved fluorescence spectra of different allophycocyanins fromMastigocladus laminosus. Biophys J 57:133–145

    CAS  Google Scholar 

  • Isono T, Katoh T (1983) Subparticles ofAnabaena phycobilisomes I. Reconstitution of allophycocyanin cores and entire phycobilisomes. Plant Cell Physiol 24:357–368

    CAS  Google Scholar 

  • Kirk JTO (1968) Studies on the dependence of chlorophyll synthesis on protein synthesis inEuglena gracilis, together with a nomogram for determination of chlorophyll concentration. Planta 78:200–207

    Article  CAS  Google Scholar 

  • Kume N, Isono T, Katoh T (1982) Stability of cyanobacterial phycobilisomes in reference to their concentration. Photobiochem Photobiophys 4:25–37

    CAS  Google Scholar 

  • Kursar TA, Alberte RS (1983) Photosynthetic unit organization in a red alga. Plant Physiol 72:409–414

    PubMed  CAS  Google Scholar 

  • Lange W, Wilhelm C, Wehrmeyer W, Mörschel E (1990) The supramolecular structure of photosystem II-phycobilisome-complexes ofPorphyridium cruentum. Bot Acta 103:250–257

    Google Scholar 

  • Lichtlé C, Thomas JC (1976) Étude ultrastructurale des thylakoides des algues à phycobiliproteines, comparison des résultats obtenus par fixation classique et cryodécapage. Phycologia 15:393–404

    Google Scholar 

  • Lundell DJ, Glazer AN (1981) Allophycocyanin B. A common subunit inSynechococcus allophycocyanin B (λmax 670) and allophycocyanin (λmax 650). J Biol Chem 256:12600–12606

    PubMed  CAS  Google Scholar 

  • Lundell DJ, Glazer AN (1983a) Molecular architecture of a light-harvesting antenna. Core substructure inSynechococcus 6301 phycobilisomes: two new allophycocyanin and allophycocyanin B complexes. J Biol Chem 258:902–908

    PubMed  CAS  Google Scholar 

  • Lundell DJ, Glazer AN (1983b) Molecular architecture of a light-harvesting antenna. Quaternary interactions in theSynechococcus 6301 phycobilisome core as revealed by partial digestion and circular dichroism studies. J Biol Chem 258:8708–8713

    PubMed  CAS  Google Scholar 

  • Manodori A, Melis A (1984) Photochemical apparatus organization inAnacystis nidulans (Cyanophyceae). Effect of CO2 concentration during cell growth. Plant Physiol 74:67–71

    Article  PubMed  CAS  Google Scholar 

  • Marsho TV, Kok B (1971) Detection and isolation of P700. Methods Enzymol 23:515–522

    Article  CAS  Google Scholar 

  • Maxson P, Sauer K, Zhou J, Bryant DA, Glazer AN (1989) Spectroscopic studies of cyanobacterial phycobilisomes lacking core polypeptides. Biochim Biophys Acta 977:40–51

    PubMed  CAS  Google Scholar 

  • Mimuro M, Lipschultz C, Gantt E (1986) Energy flow in the phycobilisome core ofNostoc sp. (MAC): two independent terminal pigments. Biochim Biophys Acta 852:126–132

    Article  CAS  Google Scholar 

  • Mörschel E, Schatz GH (1987) Correlation of photosystem-II complexes with exoplasmic freeze-fracture particles of thylakoids of the cyanobacteriumSynechococcus sp. Planta 172: 145–154

    Article  Google Scholar 

  • Mörschel E, Koller KP, Wehrmeyer W, Schneider H (1977) Biliprotein assembly in the disc-shaped phycobilisomes ofRhodella violacea. 1. Electron microscopy of phycobilisomes in situ and analysis of their architecture after isolation and negative staining. Cytobiology 16:118–129

    Google Scholar 

  • Myers J, Graham JR (1983) On the ratio of photosynthetic reaction centers RC2/RC1 inChlorella. Plant Physiol 71:440–442

    PubMed  CAS  Google Scholar 

  • Ohki K, Fujita Y (1992) Photoregulation of the phycobilisome structure during complementary chromatic adaptation in the marine cyanobacteriumPhormidium sp. C86. J Phycol 28:803–808

    Article  CAS  Google Scholar 

  • Pinter J, Provasoli L (1958) Artificial cultivation of a red-pigmented marine blue-green alga,Phormidium persicinum. J Gen Microbiol 18:190–197

    Google Scholar 

  • Redecker D, Wehrmeyer W, Reuter W (1993) Core substructure of the hemiellipsoidal phycobilisome from the red algaPorphyridium cruentum. Eur J Cell Biol 62:442–450

    PubMed  CAS  Google Scholar 

  • Reuter W, Nickel-Reuter C (1993) Molecular assembly of the phycobilisomes from the cyanobacteriumMastigocladus laminosus. J Photochem Photobiol B 18:51–66

    Article  CAS  Google Scholar 

  • Reuter W, Wehrmeyer W (1988) Core substructure inMastigocladus laminosus phycobilisomes. 1. Microheterogeneity in two of three allophycocyanin core complexes. Arch Microbiol 150:534–540

    Article  CAS  Google Scholar 

  • Reuter W, Wehrmeyer W (1990) Core substructure inMastigocladus laminosus phycobilisomes. 2. The central part of the tricylindrical core-APCM-contains the “anchor” polypeptide and no allophycocyanin B. Arch Microbiol 153:111–117

    Article  CAS  Google Scholar 

  • Reuter W, Nickel C, Wehrmeyer W (1990) Isolation of allophycocyanin B fromRhodella violacea results in a model of the core from hemidiscoidal phycobilisomes of rhodophyceae. FEBS Lett 273:155–158

    Article  PubMed  CAS  Google Scholar 

  • Tandeau de Marsac N (1977) Occurrence and nature of chromatic adaptation in cyanobacteria. J Bacteriol 130:82–91

    PubMed  CAS  Google Scholar 

  • Tandeau de Marsac N (1983) Phycobilisomes and complementary chromatic adaptation in cyanobacteria. Bull Inst Pasteur 81:201–254

    CAS  Google Scholar 

  • Tandeau de Marsac N, Houmard J (1993) Adaptation of cyanobacteria to environmental stimuli: new steps towards molecular mechanisms. FEMS Microbiol Rev 104:119–190

    Article  CAS  Google Scholar 

  • Tandeau de Marsac N, Mazel D, Damerval T, Guglielmi G Capuano V, Houmard J (1988) Photoregulation of gene expression in the filamentous cyanobacteriumCalothrix sp. PCC 7601: light-harvesting complexes and cell differentiation. Photosynthesis Res 18:99–132

    Article  Google Scholar 

  • Wehrmeyer W, Zimmermann C, Ohki K, Fujita Y (1988) On a new type of cyanobacterial phycobilisome exemplified inPhormidium persicinum. Eur J Cell Biol 46:539–546

    Google Scholar 

  • Wehrmeyer W, Mörschel E, Vogel K (1993) Core substructure in phycobilisomes of red algae. 2. The central part of the tricylindrical core-APCM-a constituent of hemidiscoidal phycobilisomes ofRhodella violacea. Eur J Cell Biol 60:203–209

    PubMed  CAS  Google Scholar 

  • Westermann M (1992) Biochemische und ultrastrukturelle Charakterisierung der hemidiscoidalen und hemiellipsoidalen Phycobilisomentypen vonPhormidium sp. (Cyanobacteria). PhD thesis. Philipps-Universität Marburg

    Google Scholar 

  • Westermann M, Reuter W, Schimek C, Wehrmeyer W (1993) Presence of both hemidiscoidal and hemiellipsoidal phycobilisomes in aPhormidium species (Cyanobacteria). Z Naturforsch [C] 48:28–34

    CAS  Google Scholar 

  • Yamanaka G, Lundell DJ, Glazer AN (1982) Molecular architecture of a light-harvesting antenna. Isolation and characterization of phycobilisome subassembly particles. J Biol Chem 257: 4077–4086

    PubMed  CAS  Google Scholar 

  • Zhao J, Zhou J, Bryant DA (1992) Energy transfer process in phycobilisomes as deduced from analyses of mutants ofSynechococcus sp. PCC 7002. In: Murata N (ed) Research in photosynthesis, vol 1. Kluwers, Dordrecht Boston London, pp 25–32

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Westermann, M., Wehrmeyer, W. A new type of complementary chromatic adaptation exemplified byPhormidium sp. C86: Changes in the number of peripheral rods and in the stoichiometry of core complexes in phycobilisomes. Arch. Microbiol. 164, 132–141 (1995). https://doi.org/10.1007/BF02525319

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02525319

Key words

Navigation