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Sites of phospholipid biosynthesis during induction of intracytoplasmic membrane formation in Rhodopseudomonas sphaeroides

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Abstract

A rapid, gratuitous and cell-division uncoupled induction of intracytoplasmic photosynthetic membrane formation was demonstrated in low-aeration suspensions of chemotrophically grown Rhodopseudomonas sphaeroides. Despite a nearly 2-fold increase in phospholipid levels, no significant increases were detected in the specific activities of CDP-1,2-diacyl-sn-glycerol:sn-glycerol-3-phosphate phosphatidyltransferase (phosphatidylglycerophosphate synthase, EC 2.7.8.5) and CDP-1,2-diacyl-sn-glycerol:L-serine O-phosphatidyltransferase (phosphatidylserine synthase, EC 2.7.8.8), the first committed enzymes of anionic and zwitterionic phospholipid biosyntheses, respectively. The distribution of phosphatidylglycerophosphate and phosphatidylserine synthase activities after rate-zone sedimentation of cell-free extracts indicated that intracytoplasmic membrane phospholipids were synthesized mainly within distinct domains of the conserved cytoplasmic membrane. Labeling studies with 32Pi and L-[3H]phenylalanine suggested that preexisting phospholipid was utilized initially as the matrix for insertion of intracytoplasmic membrane protein that was synthesized and assembled de novo during induction.

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Abbreviations

BChl:

bacteriochlorophyll a

B800-850, B875:

peripheral and core light-harvesting BChl-protein complexes, respectively, identified by near-IR absorption maxima

References

  • Birrell GB, Sistrom WR, Griffith OH (1978) Lipid-protein associations in chromatophores from the photosynthetic bacterium Rhodopseudomonas sphaeroides. Biochemistry 17:3768–3773

    Google Scholar 

  • Broglie RM, Niederman RA (1979) Membranes of Rhodopseudomonas sphaeroides: Effect of cerulenin on assembly of chromatophore membrane. J Bacteriol 138:788–798

    Google Scholar 

  • Brown AE, Eiserling FA, Lascelles J (1972) Bacteriochlorophyll synthesis and the ultrastructure of wild-type and mutant strains of Rhodopseudomonas sphaeroides. Plant Physiol 50:743–746

    Google Scholar 

  • Cain BD, Deal CD, Fraley RT, Kaplan S (1981) In vivo intermembrane transfer of phospholipids in the photosynthetic bacterium Rhodopseudomonas sphaeroides J Bacteriol 145:1154–1166

    Google Scholar 

  • Cain BD, Singer M, Donohue TJ, Kaplan S (1983) In vivo metabolic intermediates of phospholipid biosynthesis in Rhodopseudomonas sphaeroides. J Bacteriol 156:375–385

    Google Scholar 

  • Cain BD, Donohue TJ, Shepherd WD, Kaplan S (1984) Localization of the phospholipid biosynthetic enzyme activities in cell-free fractions derived from Rhodopseudomonas sphaeroides. J Biol Chem 259:942–948

    Google Scholar 

  • Chory J, Donohue TJ, Varga AR, Staehelin LA, Kaplan S (1984) Induction of the photosynthetic membranes of Rhodopseudomonas sphaeroides: biochemical and morphological studies. J Bacteriol 159:540–554

    Google Scholar 

  • Clayton RK (1966) Spectroscopic analysis of bacteriochlorophyll in vitro and in vivo. Photochem Photobiol 5:669–677

    Google Scholar 

  • Cooper CL, Lueking DR (1984) Localization and characterization of the sn-glycerol-3-phosphate acyltransferase in Rhodopseudomonas sphaeroides. J Lipid Res 25:1222–1232

    Google Scholar 

  • Dierstein R, Drews G (1982) Membrane differentiation and assembly of the pigment-protein complexes of the photosynthetic bacterium Rhodopseudomonas capsulata. In: Akoyunoglou G, Evangelopoulos AE, Georgatsos J, Palaiologos G, Trakatellis A, Tsiganos CP (eds) Cell function and differentiation, part B. Alan R. Liss, New York, pp 247–256

    Google Scholar 

  • Drews G (1982) Composition and development of the bacterial photosynthetic apparatus. In: Kaplan NO, Robinson A (eds) From cyclotrons to cytochromes. Essays in molecular biology and chemistry. Academic Press, New York, pp 355–366

    Google Scholar 

  • Drews G, Oelze J (1981) Organization and differentiation of membranes of phototrophic bacteria. Adv Microbial Physiol 22:1–92

    Google Scholar 

  • Hirabayashi T, Larson TJ, Dowhan W (1976) Membrane-associated phosphatidylglycerophosphate synthetase from Escherichia coli: Purification by substrate affinity chromatography on cytidine 5′-diphospho-1,2-diacyl-sn-glycerol sepharose. Biochemistry 15:5205–5211

    Google Scholar 

  • Inamine GS, Reilly PA, Niederman RA (1984a) Differential protein insertion into developing photosynthetic membrane regions of Rhodopseudomonas sphaeroides. J Cell Biochem 24:69–77

    Google Scholar 

  • Inamine GS, Van Houten J, Niederman RA (1984b) Intracellular localization of photosynthetic membrane growth initiation sites in Rhodopseudomonas sphaeroides. J Bacteriol 158:425–429

    Google Scholar 

  • Kaplan S, Arntzen CJ (1982) Photosynthetic membrane structure and function. In: Govindjee (ed) Photosynthesis, vol. 1. Academic Press, New York, pp 65–151

    Google Scholar 

  • Kell DB (1984) Diffusion of protein complexes in prokaryotic membranes: fast, free, random or directed? Trends Biochem Sci 9:86–88

    Google Scholar 

  • Lascelles J, Szilagyi JF (1965) Phospholipid synthesis by Rhodopseudomonas sphaeroides in relation to the formation of photosynthetic pigments. J Gen Microbiol 38:55–64

    Google Scholar 

  • Lueking DR, Fraley RT, Kaplan S (1978) Intracytoplasmic membrane synthesis in synchronous cell populations of Rhodopseudomonas sphaeroides. Fate of “old” and “new” membrane. J Biol Chem 253:451–457

    Google Scholar 

  • Niederman RA, Gibson KD (1978) Isolation and physicochemical properties of membranes from purple photosynthetic bacteria. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum Publishing Corp, New York, pp 79–118

    Google Scholar 

  • Niederman RA, Mallon DE, Langan JJ (1976) Membranes of Rhodopseudomonas sphaeroides. IV. Assembly of chromatophores in low aeration cell suspensions. Biochim Biophys Acta 440:429–447

    Google Scholar 

  • Niederman RA, Mallon DE, Parks LC (1979) Membranes of Rhodopseudomonas sphaeroides. VI. Isolation of a fraction enriched in newly synthesized bacteriochlorophyll a-protein complexes. Biochim Biophys Acta 555:210–220

    Google Scholar 

  • Niederman RA, Hunter CN, Inamine GS, Mallon DE (1981) Development of the bacterial photosynthetic apparatus. In: Akoyunoglou G (ed) Photosynthesis, vol 5. Chloroplast development. Balaban, Philadelphia, pp 663–674

    Google Scholar 

  • Onishi JC, Niederman RA (1982) Rhodopseudomonas sphaeroides membranes: Alterations in phospholipid composition in aerobically and phototrophically grown cells. J Bacteriol 149:831–839

    Google Scholar 

  • Parks LC, Niederman RA (1978) Membranes of Rhodopseudomonas sphaeroides. V. Identification of bacteriochlorophyll a-depleted cytoplasmic membrane in phototrophically grown cells. Biochim Biophys Acta 511:70–82

    Google Scholar 

  • Pennoyer JD, Niederman RA (1984) Fusion of liposomes to photosynthetic membranes of Rhodopseudomonas sphaeroides: Effect on structural organization of light-harvesting system. In: Siegenthaler PA, Eichenberger W (eds) Structure, function and metabolism of plant lipids. Elsevier Science Publishers, Amsterdam, pp 437–441

    Google Scholar 

  • Peters GA, Cellarius RA (1972) Photosynthetic membrane development in Rhodopseudomonas sphaeroides. J Bioenerg 3:345–359

    Google Scholar 

  • Radcliffe CW, Niederman RA (1984) Intracellular localization of membrane-associated phosphatidylserine synthase in Rhodopseudomonas sphaeroides. In: Siegenthaler PA, Eichenberger W (eds) Structure, function and metabolism of plant lipids. Elsevier Science Publishers, Amsterdam, pp 319–323

    Google Scholar 

  • Radcliffe CW, Pennoyer JD, Broglie RM, Niederman RA (1984) Associations of pigment-proteins and phospholipids into specific domains in Rhodopseudomonas sphaeroides photosynthetic membranes as determined by lithium dodecyl sulfate/polyacrylamide gel electrophoresis. In: Sybesma C (ed) Advances in photosynthesis research, vol II. Martinus Nijhoff/Dr. W. Junk Publishers, The Hague Boston Lancaster, pp 215–219

    Google Scholar 

  • Raetz CRH, Kennedy EP (1972) The association of phosphatidylserine synthetase with ribosomes in extracts of Escherichia coli. J Biol Chem 247:2008–2014

    Google Scholar 

  • Raetz CRH, Larson TJ, Dowhan W (1977) Gene cloning for the isolation of enzymes of membrane lipid synthesis: phosphatidylserine synthase overproduction in Escherichia coli. Proc Natl Acad Sci USA 74:1412–1416

    Google Scholar 

  • Takemoto J, Lascelles J (1973) Coupling between bacterio-chlorophyll and membrane protein synthesis in Rhodopseudomonas sphaeroides. Proc Natl Acad Sci USA 70:799–803

    Google Scholar 

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Author notes

  1. Richard M. Broglie

    Present address: Laboratory of Plant Molecular Biology, The Rockefeller University, 10021, New York, NY, USA

Authors and Affiliations

  1. Department of Biochemistry, Rutgers University, P.O. Box 1059, 08854, Piscataway, NJ, USA

    Cynthia W. Radcliffe, Richard M. Broglie & Robert A. Niederman

Authors
  1. Cynthia W. Radcliffe
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  2. Richard M. Broglie
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  3. Robert A. Niederman
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This paper is dedicated to Professor Gerhart Drews on the occasion of his sixtieth birthday

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Radcliffe, C.W., Broglie, R.M. & Niederman, R.A. Sites of phospholipid biosynthesis during induction of intracytoplasmic membrane formation in Rhodopseudomonas sphaeroides . Arch. Microbiol. 142, 136–140 (1985). https://doi.org/10.1007/BF00447056

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  • DOI: https://doi.org/10.1007/BF00447056

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