Molecular composition of cyanobacterial phycobilisomes* (phycobiliproteins/polyacrylamide gel electrophoresis/cyanobacteria/chromatic adaptation)
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1 Proc. Natl. Acad. Sci. USA Vol. 74, No. 4, pp , April 1977 Cell Biology Molecular composition of cyanobacterial phycobilisomes* (phycobiliproteins/polyacrylamide gel electrophoresis/cyanobacteria/chromatic adaptation) N. TANDEAU DE MARSAC AND G. COHEN-BAZIRE Departement de Biochimie et Gknktique Microbienne, Institut Pasteur, 28 rue du Dr. Roux, Paris Cedex 15, France Communicated by H. A. Barker, February 3, 1977 ABSTRACT Phycobilisomes isolated from eight different of colorless polypeptides, all of higher molecular weight than species of cyanobacteria contain, in addition to the light-harvesting phycobiliproteins, a small number of colorless poly- the chromopolypeptide subunits of the phycobiliproteins. peptides with molecular weights higher than those of the chromopolypeptide subunits of the phycobiliproteins. In the MATERIALS AND METHODS phycobilisomes of the species examined, from four to nine colorless polypeptides were resolved by sodium dodecyl sulfate/ Biological Material. Phycobilisomes were isolated from polyacrylamide gel electrophoresis. Those of highest molecular eight species of cyanobacteria maintained in the culture collection of our laboratory (Table 1). Cultures were grown pho- weight (7,-12,) also occurred in the washed membrane fraction of the cell and may therefore be derived from the thylakoids, to which the phycobilisomes are attached in vivo. toautotrophically at room temperature (2-25 ) in medium Colorless polypeptides of lesser molecular BG-li (1) and harvested while still weight (3,- growing actively. Most 7,) appeared to be specific constituents of the phycobilisome. In strains of cyanobacteria that adapt chromatically, their fluorescent lamps). Some were grown in chromatic light pro- cultures were grown in white light (Osram white Universal synthesis, like that of the major phycobiliproteins, is regulated duced by the interposition of a green or red plastic filter (9) by light quality. between the fluorescent light source and the culture vessel. Extraction and Isolation of Phycobilisomes. Phycobilisomes were prepared by a procedure similar to that developed In cyanobacteria, a major part of the light-harvesting pigment system is located in a special organelle, the phycobilisome (1). by Gray and Gantt (6). Organisms harvested by centrifugation Regular rows of phycobilisomes, each some 4 nm in diameter, were resuspended in.5 M ammonium phosphate buffer (ph are attached to the external surface of the thylakoid which 7.) at a concentration of approximately.1 g (wet weight)/ml. contains the other elements of the photosynthetic apparatus. The suspension was then broken in a French pressure cell under Three phycobiliproteins-allophycocyanin B (Xmax 671 nm), 13 atm. The extract was collected and incubated for 3 min allophycocyanin (Xmax 65 nm), and phycocyanin (Xmax 62 at room temperature in the presence of 1% (vol/vol) Triton nm)-are always present in the phycobilisome (2). They are X-1. In a few experiments, the Triton X-1 treatment was accompanied in many cyanobacteria by other phycobiliproteins omitted. All subsequent operations were conducted at 4 C. The with absorption maxima at shorter wavelengths: phycoerythrins extract was clarified by centrifugation at 3, X g for 3 min. (Amax 5-58 nm) or the recently discovered (3) pigment Aliquots (1.5 ml) of the clarified supernatant were then layered phycoerythrocyanin (,max 568 nm). Quantum energy absorbed onto discontinuous sucrose gradients, prepared with 2, 5, 5, 4, by any phycobilisomal pigment is channeled by radiationless and 3 ml, respectively, of 2., 1.,.75,.5, and.25 M sucrose transfer to the photochemical reaction centers of the thylakoid dissolved in.75 M Na,K phosphate buffer (ph 7.). After (4). Within the phycobilisome, radiationless energy transfer centrifugation at 65, X g for hr, the phycobilisome takes place through the sequence: phycoerythrin (or phycoerythrocyanin) -- phycocyanin - o fraction was eluted and freed of sucrose by passage through a allophycocyanin allophycocyanin B (ref. 5; Ley, Bryant, Glazer, and Butler, personal buffer. Many phycobilisome preparations were subsequently column of Sephadex G-25 previously equilibrated with the same communication). concentrated by precipitation with ammonium sulfate (3% Phycobilisomes can be extracted from the cell in a seemingly saturation) and then chromatographed on a Bio-Gel A-15 column equilibrated with the same buffer. intact state with a phosphate buffer of high ionic strength and subsequently separated from other cell components by differential centrifugation (6). Dilution of the solvent causes rapid lyzed on sodium dodecyl sulfate (NaDodSO4)/polyacrylamide Analysis of Polypeptide Composition. Proteins were ana- disaggregation of the phycobilisomes, accompanied by the slab gels with the discontinuous buffer system described by uncoupling of radiationless energy transfer between the constituent phycobiliproteins (7). were prepared by diluting a stock solution containing 3% Laemmli () and the apparatus described by Studier (12). Gels It has been reported that the protein content of phycobilisomes extracted from the red alga Porphyridium can be enacrylamide. The resolving gel, 2% (wt/vol) acrylamide con- (wt/vol) acrylamide and.1% (wt/vol) N,N'-bismethylenetirely accounted for by phycobiliproteins (8); and only traces taining.375 M Tris-HCI (ph 8.8) and.1% (wt/vol) NaDodof other proteins have been detected in phycobilisomes extracted from a cyanobacterium, Nostoc sp. (6). We report here methylethylenediamine and.5% (wt/vol) ammonium per- SO4, was polymerized with.5% (vol/vol) N,N,N',N'-tetra- that the protein composition of cyanobacterial phy~obilisomes sulfate. The stacking gel, 6% (wt/vol) acrylamide, contained is in fact considerably more complex. About 15% of the total.125 M Tris-HCl (ph 6.8) and.1% NaDodSO4 and was polymerized with.6% (vol/vol) N,N,N',N'-tetramethylethy- protein in phycobilisomes is accounted for by a small number Abbreviation: NaDodSO4, sodium dodecyl sulfate. lenediamine and.6% (wt/vol) ammonium persulfate. * A preliminary account of this work was presented at the Second International Symposium on Photosynthetic Prokaryotes, Dundee, Na,K phosphate buffer (ph 7.) or against distilled water and Prior to electrophoresis, samples were dialyzed against 5 mm Scotland, August This work will be part of the Doctoral dissertation of N. Tandeau de Marsac. order to obtain a solution containing.5-1 mg of protein per ml. concentrated, if necessary, with Aquacide (Calbiochem) in 1635
2 1636 Cell Biology: de Marsac and Cohen-Bazire Proc. Nati. Acad. Sci. USA 74 (1977) Table 1. Strain designations and some properties of cyanobacteria used as sources of phycobilisomes Phycobiliproteins synthesizedt Photoregulation of ATCC* phycobiliprotein no. PE PEC PC AP synthesis (9) Unicellular cyanobacteria Synechococcus Synechocystis Synechocystis Gloeobacter Chamaesiphon Filamentous cyanobacteria LPPt group Anabaena Fremyella * American Type Culture Collection. t PE, phycoerythrin; PEC, phycoerythrocyanin; PC, phycocyanin; AP, allophycocyanin. I Lyngbya-Plectonema-Phormidium. Mr 12, 7, Samples were diluted with an equal volume of.65 M Tris- HCI (ph 6.8) containing 2% (wt/vol) NaDodSO4, 5% (vol/vol) 2-mercaptoethanol, and 1% (vol/vol) glycerol and immersed in boiling water for 3 min. Samples (5-5,l) containing not more than 15,gg of protein were electrophoresed for 15 hr at a constant voltage of 3 V in.25 M Tris buffer (ph 8.3) containing.192 M glycine and.1% (wt/vol) NaDodSO4. The gels were fixed in 5% trichloroacetic acid for 2 hr and stained for 1 hr at room temperature with.1% (wt/vol) Coomassie brilliant blue R25 dissolved in 5% (wt/vol) trichloroacetic acid. The destaining solution contained 5% (vol/vol) absolute methanol and 7.5% (vol/vol) glacial acetic acid. Stained gels were examined with an automatic gel scanner (Vernon) fitted with a filter transmitting in the range nm. The relative contribution of each polypeptide peak was estimated by measurement of the total peak area of the gel scan. Protein Determinations. Total protein was determined by the method of Lowry et al. (13) with bovine serum albumin as standard. The contents of phycoerythrin, phycocyanin, and allophycocyanin in isolated phycobilisomes were determined by measuring the absorbancy at 565, 62, and 652 nm, respectively, of samples diluted in.1 M Na phosphate buffer (ph 7.) containing.15 M NaCl (1). RESULTS Fig. 1 shows NaDodSO4/acrylamide gel electropherograms of phycobilisomes isolated from seven species of cyanobacteria grown in white light. The polypeptides of group (molecular weight, 16,-22,) which were only partly resolved in these electropherograms, consisted of the a and,b subunits of the phycobiliproteins, identified by their intrinsic color before staining. Polypeptides of higher molecular weight (groups I-) were apparent only after Coomassie blue staining. The various phycobilisome preparations examined contain four to nine major colorless polypeptides that accounted for 14-18% of the total stainable material on the gels. If the treatment with Triton X-1 was omitted from the preparative procedure, the yield of phycobilisomes was greatly decreased; however, their molecular composition was identical with that of phycobilisomes extracted in the presence of the detergent. Are the colorless polypeptides structural components of the phycobilisome, 4*NMNNM '-Npmgmk. - 3, _ - 25,, 15, Idemoa FIG. 1. NaDodSO4/polyacrylamide gel electropherograms of isolated phycobilisomes prepared from seven different cyanobacteria grown in white light. Molecular weights (Mr) were determined from a standard calibration curve using as markers: f3-galactosidase (13,), bovine serum albumin (68,), catalase (57,), ovalbumin (43,), chymotrypsinogen A (25,7), f-lactoglobulin (17,4), lysozyme (14,3). The electropherograms shown are taken from four separate gel electrophoreses, in which the extents of migration of the polypeptides differed.
3 Cell Biology: de Marsac and Cohen-Bazire Proc. Natl. Acad. Sci. USA 74 (1977) 1637 '5 4 E Ċ n 3 La c 2 (1 w a a. 2 a. U ee a 3 cn xrl 2 gj I 'E) 1n cn -J O u 5 1 IS FRACTION NUMBER FIG. 2. Polypeptide compositions of fractions eluted from a discontinuous sucrose gradient overlaid with a cell-free extract of strain 749 grown under white light. Each fraction was analyzed by NaDodSO4/polyacrylamide gel electrophoresis, the quantity of individual polypeptides or groups of polypeptides being estimated from stained gel scans. The amounts of total chromopolypeptides (-) and total colorless polypeptides (O--- -) are expressed in arbitrary units per fraction (1 ml) eluted from the sucrose gradient. thylakoidal proteins detached together with the phycobilisomes, or merely contaminating soluble proteins? The results of a series of experiments undertaken in an attempt to answer this question are summarized below. The polypeptide composition of phycobilisomes isolated by elution from a sucrose gradient was unchanged both after precipitation with ammonium sulfate at 3% saturation and after passage through a Bio-Gel A-15 molecular sieve. Such experiments were performed with phycobilisomes isolated from five different species of cyanobacteria. The isolated phycobilisomes of strain 749 contained six colorless polypeptides (Fig. 1). The relative amounts of these colorless polypeptides and of total chromopolypeptides were determined from gel scans on successive fractions eluted from a sucrose gradient after centrifugation of an extract of strain 749 (Fig. 2). The distributions through the gradient of the individual colorless polypeptides are shown in Fig. 3. In the region of the gradient that contains the phycobilisomes (fractions 7-: M sucrose) there was excellent correlation between the distributions of chromopolypeptides and colorless phycobilisomal polypeptides. Light quality affects differentially the rates of phycoerythrin and phycocyanin synthesis in strains 749 and 761 (9, 14). Phycobilisomes prepared from these strains after growth in white, red, and green light differed markedly in their phycobiliprotein composition. "Green-light" phycobilisomes had a high phycoerythrin:phycocyanin ratio, "white-light" phycobilisomes had a somewhat lower phycoerythrin:phycocyanin ratio, and "red-light" phycobilisomes were virtually devoid of phycoerythrin. These light-induced modifications of the major phycobilisomal light-harvesting proteins were accompanied by marked changes in the relative concentrations of the colorless group II polypeptides (Fig. 4). The results of a semiquantitative analysis of the composition 5 IQ 15. FRACTION NUMBER FIG. 3. Distributions through a sucrose gradient of the individual colorless polypeptides associated with the phycobilisomes of strain 749. Data from the experiment described in Fig. 2. of phycobilisomes prepared from strain 749 after growth in white, green, and red light are presented in Fig. 5 and Table 2. In all three preparations, the group II polypeptides collectively accounted for the same fraction (approximately 1%) of total phycobilisomal protein. In red-light phycobilisomes, which contained no phycoerythrin, polypeptide 5 was barely detectable, polypeptides 3 and 4 accounting for over 95% of the group II components. In green-light phycobilisomes, of which phycoerythrin was the major phycobiliprotein (51% of the total), polypeptide 5 accounted for 8% of the group II components. White-light phycobilisomes had an intermediate composition with respect both to phycobiliproteins and to group II polypeptides. The physical integrity of the phycobiisome is maintained only in buffers of high ionic strength. Consequently, if cells are broken in buffers of low ionic strength, the constituent proteins of the phycobilisome pass into solution and become mixed with other soluble cytoplasmic proteins in the resulting extract. The bulk soluble proteins of such an extract can be subsequently separated by differential centrifugation from the membrane fraction, which contains the thylakoid-associated proteins. For two cyanobacteria, we compared the polypeptide composition of isolated phycobilisomes with the polypeptide compositions of low-ionic-strength extracts and of the soluble and membrane fractions prepared from them (Fig. 6). In both cyanobacteria, the group II polypeptides, as well as the bulk of the chromopolypeptides, occurred in the soluble fraction of the lowionic-strength extract. The group polypeptide, present in the phycobilisomes of only one of these strains (761), was
4 1638 Cell Biology: de Marsac and Cohen-Bazire Proc. Natl. Acad. Sci. USA 74 (1977) Mr 12, 7, - 3, -I- 25, p 15, -- I R G R G FIG. 4. NaDodSO4/polyacrylamide gel electropherograms of isolated phycobilisomes prepared from two chromatically adapting cyanobacteria, strains 749 and 761, after growth in red (R) and green (G) light. Note the analogous light-induced changes in the relative amounts of the group II polypeptides. Mr, molecular weight. likewise associated with the soluble fraction. On the other hand, the group I polypeptides of both strains were largely, and perhaps exclusively, located in the membrane fraction of the low-ionic-strength extract. DISCUSSION In view of earlier reports (6, 8) that nearly all the protein content of isolated phycobilisomes is accounted for by phycobiliproteins, our observation that colorless polypeptides account for about 15% of the total protein of the cyanobacterial phycobilisome was wholly unexpected. In the seven cyanobacteria studied, this material consisted of a small number of polypeptides: four to nine components are resolvable by NaDodSO4/polyacrylamide gel electrophoresis. It is improbable that these polypeptides are derived from contaminating soluble cytoplasmic proteins in the preparations examined. The strongest evidence for their specific association with the phycobilisome was obtained by an Il II m tv 4-1~ ~ ~ ~ I Molecular weights (x 1 3) of marker proteins FIG. 5. Scans of Coomassie blue-stained NaDodSO4/polyacrylamide gel electropherograms of phycobilisomes prepared from cells of strain 749 after growth under white light, green light, and red light. Peaks 1-6 represent the colorless polypeptides of groups I (1 and 2), II (3 to 5), and (6). The broad band containing two peaks (7 and 8) of unequal height, extending over the molecular weight range 16,-22,, reflects the overlapping absorbances of the chromopolypeptides derived from the phycobiliproteins. The predominance of phycoerythrin in "green-light" phycobilisomes is reflected by an increase in absorbance at the higher end of the molecular weight range, since the mean subunit molecular weight of it is greater than that of phycocyanin and allophycocyanin. analysis of the polypeptide compositions of successive fractions eluted from a sucrose gradient after centrifugation of an extract of strain 749. This analysis revealed a good correlation between the distribution through the gradient of the chromopolypeptides derived from the phycobiliproteins and of each of the six colorless polypeptides associated with isolated phycobilisome. There is no obvious explanation for the difference between our findings concerning the molecular composition of the phycobilisome and those of earlier workers (6, 8). Nevertheless, the discrepancy should be easily resolved. As our data show, colorless proteins represent approximately 15% of total.phyco- Table 2. Chemical composition of phycobilisomes isolated from strain 749 after growth with three light sources of different spectral character % of total phycobilisomal protein* All % of total group II % of total colorless Polypeptide groups: polypeptides* phycobiliproteinst poly- Grown under peptides I II AP PC PE White light Green light Red light * Estimated from scans of gel electropherograms (see Materials and Methods). t Estimated spectrophotometrically (see Materials and Methods). AP, allophycocyanin; PC, phycocyanin; PE, phycoerythrin.
5 Cell Biology: -. de Marsac and Cohen-Bazire W- -4 A B C D A B FIG. 6. NaDodSO4/polyacrylamide gel electropherograms of crude cell-free extracts (A), washed membrane fractions (B), soluble protein fractions (C), and isolated phycobilisomes (D) prepared from strain 6312 grown under white light and from strain 761 grown under red light. See text for explanations. bilisomal protein. These components should be readily detectable by the analytical procedures described here in all preparations of phycobilisomes, irrespective of their biological source and mode of isolation. In view of the function of the phycobilisome as a light-harvesting organelle, two possible roles for its colorless protein constituents can be envisaged: attachment of the organelle to a specific site on the thylakoid membrane and positioning of the constituent light-harvesting pigments within the phycobilisome. Because the group I polypeptides appear also to be present in the washed membrane fraction prepared from cells after extraction with a buffer of low ionic strength, they may serve to attach the phycobilisome to the thylakoid. The group II polypeptides, on the other hand, are probably involved in the assembly and positioning of the phycobiliproteins. Like the phycobiliproteins, they are located exclusively in the soluble fraction of extracts prepared at low ionic strength. Furthermore, in chromatically adapting strains, changes in the relative Proc. Nati. Acad. Sci. USA 74 (1977) 1639 amounts of the two major phycobiliproteins are correlated with changes in the relative amounts of individual group II polypeptides. Photoregulation thus governs the synthesis both of chromoproteins and of certain colorless protein components of the phycobilisome. We thank Dr. R. Haselkorn for helpful discussions and Dr. R. Y. Stanier for advice and encouragement. The skillful assistance of Miss A. M. Castets is gratefully acknowledged. This work was supported by grants from the "Centre National de la Recherche Scientifique" ERA no. 398 and by the "Delegation Generale a la Recherche Scientifique et Technique" (Contract ). 1. Gray, B. H., Lipschultz, C. A. & Gantt, E. (1973) "Phycobilisomes from a blue-green alga Nostoc sp.," J. Bacteriol. 6, Glazer, A. N. & Bryant, D. A. (1975) "Allophycocyanin B (Amax 671, 618 nm): A new cyanobacterial phycobiliprotein," Arch. Microbiol. 14, Bryant, D. A., Glazer, A. N. & Eiserling, F. A. (1976) "Characterization and structural properties of the major biliproteins of Anabaena sp.," Arch Microbiol., Haxo, F. T. (196) "The wavelength dependence of photosynthesis and the role of accessory pigments," in Comparative Biochemistry of Photoreactive Pigments, ed. Allen, M. B. (Academic Press, New York), pp Gantt, E. & Lipschultz, C. A. (1973) "Energy transfer in phycobilisomes from phycoerythrin to allophycocyanin," Biochim. Biophys. Acta 292, Gray, B. H. & Gantt, E. (1975) "Spectral properties of phycobilisomes and phycobiliproteins from the blue-green alga Nostoc sp.," Photochem. Photobiol. 21, Gantt, E., Lipschultz, C. A. & Zilinkas, B. (1976) "Further evidence for a phycobilisome model from selective dissociation, fluorescence emission, immunoprecipitation and electron microscopy," Biochim. Biophys. Acta 43, Gantt, E. & Lipschultz, C. A. (1974) "Phycobilisomes of Porphyridium cruentum: pigment analysis," Biochemistry 13, Tandeau de Marsac, N. (1977) "The occurrence and nature of chromatic adaptation in cyanobacteria," J. Bacteriol., in press. 1. Stanier, R. Y., Kunisawa, R., Mandel, M. & Cohen-Bazire, G. (1971) "Purification and properties of unicellular blue-green algae (order Chroococales)," Bacteriol. Rev. 35, Laemmli, U. K. (197) "Cleavage of structural proteins during the assembly of the head of bacteriophage T4," Nature 227, Studier, F. W. (1973) "Analysis of bacteriophage T7 early RNAs and proteins on slab gels," J. Mol. Biol. 79, Lowry,. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. (1951) "Protein measurement with the Folin phenol reagent," J. Biol. Chem. 193, Bennett, A. & Bogorad, L. (1973) "Complementary chromatic adaptation in a filamentous blue-green alga," J. Cell Biol. 58,
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