Skip to main content
SpringerLink
Log in

Heterogeneity of carotenoid content and composition in LH2 of the purple sulphur bacterium Allochromatium minutissimum grown under carotenoid-biosynthesis inhibition

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

Abstract

The effects brought about by growing Allochromatium (Alc.) minutissimum in the presence of different concentrations of the carotenoid (Car) biosynthetic inhibitor diphenylamine (DPA) have been investigated. A decrease of Car content (from ~70% to >5%) in the membranes was accompanied by an increase of the percentage of (immature) Cars with reduced numbers of conjugated C=C bonds (from neurosporene to phytoene). Based on the obtained results and the analysis of literature data, the conclusion is reached that accumulation of phytoene during inhibition did not occur. Surprisingly, DPA inhibited phytoene synthase instead of phytoene desaturase as generally assumed. The distribution of Cars in peripheral antenna (LH2) complexes and their effect on the stability of LH2 has been investigated using absorption spectroscopy and HPLC analysis. Heterogeneity of Car composition and contents in the LH2 pool is revealed. The Car contents in LH2 varied widely from control levels to complete absence. According to common view, the assembly of LH2 occurs only in the presence of Cars. Here, we show that the LH2 can be assembled without any Cars. The presence of Cars, however, is important for structural stability of LH2 complexes.

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

Similar content being viewed by others

Abbreviations

BChl:

Bacteriochlorophyll

Car:

Carotenoid

DM:

n-Dodecyl-β-d-maltoside

DPA:

Diphenylamine

FP:

Free pigments

HPLC:

High performance liquid chromatography

LH1, LH2:

Core and peripheral light-harvesting complexes

RC:

Reaction centre

Alc. :

Allochromatium

References

  • Bartley GE, Scolnik PA (1989) Carotenoid biosynthesis in photosynthetic bacteria. Genetic characterization of the Rhodobacter capsulatus CrtI protein. J Biol Chem 264:13109–13113

    PubMed  CAS  Google Scholar 

  • Bramley PM (1993) Inhibition of carotenoid biosynthesis. In: Young A, Britton G (eds) Carotenoids in photosynthesis. Chapmann & Hall, London, pp 127–159

    Google Scholar 

  • Britton G, Liaaen-Jensen S, Pfander H (2004) Carotenoids. Birkhäuser Verlag, Basel

    Google Scholar 

  • Cogdell RJ, Gall A, Köhler J (2006) The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes. Q Rev Biophys 39:227–324. doi:10.1017/S0033583506004434

    Article  PubMed  CAS  Google Scholar 

  • Cohen-Bazire G, Stanier RY (1958) Inhibition of carotenoid synthesis in photosynthetic bacteria. Specific inhibition of carotenoid synthesis in a photosynthetic bacterium and its physiological consequences. Nature 181:250–252. doi:10.1038/181250a0

    Article  PubMed  CAS  Google Scholar 

  • Davidson E, Cogdell RJ (1981) The polypeptide composition of the B850 light-harvesting pigment–protein complex from Rhodopseudomonas sphaeroides R26.1. FEBS Lett 132:81–84. doi:10.1016/0014-5793(81)80432-2

    Article  CAS  Google Scholar 

  • Davies BH (1970a) A novel sequence for phytoene dehydrogenation in Rhodospirillum rubrum. Biochem J 116:93–99

    PubMed  CAS  Google Scholar 

  • Davies BH (1970b) Alternative pathways of spirilloxanthin biosynthesis in Rhodospirillum rubrum. Biochem J 116:101–110

    PubMed  CAS  Google Scholar 

  • Davies BH, Köst H-P (1988) CRC handbook of chromatography. In CRC series in chromatography. CRC Press, Boca Raton

    Google Scholar 

  • Drews G (1985) Structure and functional organization of light-harvesting complexes and photochemical reaction centers in membranes of phototrophic bacteria. Microbiol Rev 49:59–70

    PubMed  CAS  Google Scholar 

  • Erokhin YE, Moskalenko AA (1973) Characterization of the proteins of the Chromatium pigment–lipoprotein complexes (number of chains and molecular weights). Dokl Akad Nauk SSSR 212:495–498 (in Russian)

    PubMed  CAS  Google Scholar 

  • Fuller RC, Anderson IC (1958) Inhibition of carotenoid synthesis in photosynthetic bacteria. Suppression of carotenoid synthesis and its effect on the activity of photosynthetic bacterial chromatophores. Nature 181:252–254. doi:10.1038/181252a0

    Article  PubMed  CAS  Google Scholar 

  • Gall A, Cogdell RJ, Robert B (2003) Influence of carotenoid molecules on the structure of the bacteriochlorophyll binding site in peripheral light-harvesting proteins from Rhodobacter sphaeroides. Biochemistry 42:7252–7258. doi:10.1021/bi0268293

    Article  PubMed  CAS  Google Scholar 

  • Gall A, Henry S, Takaichi S, Robert B, Cogdell RJ (2005) Preferential uptake of coloured carotenoids occurs in the LH2 complexes from nonsulphur purple bacteria under carotenoid-limiting conditions. Photosynth Res 86:25–35. doi:10.1007/s11120-005-3481-0

    Article  PubMed  CAS  Google Scholar 

  • Goodwin TW (1956) The carotenoids of photosynthetic bacteria. The carotenoids of a number of non-sulphur purple bacteria (Athiorodaceae). Arch Microbiol 24:313–322. doi:10.1007/BF00693102

    CAS  Google Scholar 

  • Goodwin TW, Land DG (1956) The carotenoids of photosynthetic bacteria. 1. The nature of the carotenoids pigments in a halophilic photosynthetic bacterium (Chromatium sp.). Arch Microbiol 24:305–312. doi:10.1007/BF00419015

    CAS  Google Scholar 

  • Goodwin TW, Osman HG (1953) Studies in carotenogenesis. 9. General cultural conditions controlling carotenoid (spirilloxanthin) synthesis in the photosynthetic bacterium Rhodospirillum rubrum. Biochem J 53:541–546

    PubMed  CAS  Google Scholar 

  • Goodwin TW, Osman HG (1954) Studies in carotenogenesis. Spirilloxanthin synthesis by washed cells of Rhodospirillum rubrum. Biochem J 56:222–230

    PubMed  CAS  Google Scholar 

  • Griffiths M, Stanier RY (1956) Some mutational changes in the photosynthetic pigment system of Rhodopseudomonas sphaeroides. J Gen Microbiol 14:698–715

    PubMed  CAS  Google Scholar 

  • Griffiths M, Sistrom WR, Cohen-Bazire G, Stainer RY (1955) Functions of carotenoids in photosynthesis. Nature 176:1211–1214. doi:10.1038/1761211a0

    Article  PubMed  CAS  Google Scholar 

  • Koepke J, Hu X, Muenke C, Schulten K, Michel H (1996) The crystal structure of the light-harvesting complex II (B800–850) from Rhodospirillum molischianum. Structure 4:581–597. doi:10.1016/S0969-2126(96)00063-9

    Article  PubMed  CAS  Google Scholar 

  • Krikunova M, Kummrow A, Voigt B, Rini M, Lokstein H, Moskalenko A, Scheer H, Razjivin A, Leupold D (2002) Fluorescence of native and carotenoid-depleted LH2 from Chromatium minutissimum, originating from simultaneous two-photon absorption in the spectral range of the presumed (optically ‘dark’) S1 state of carotenoids. FEBS Lett 528:227–229. doi:10.1016/S0014-5793(02)03315-X

    Article  PubMed  CAS  Google Scholar 

  • Hunter CN (1995) Genetic manipulation of the antenna complexes of purple bacteria. In: Blakenship RE, Madigan MT, Bauer CE (eds) Anoxygenic Photosynthetic Bacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 473–501

    Google Scholar 

  • Lang HP, Hunter CN (1994) The relationship between carotenoid biosynthesis and the assembly of the light harvesting LH2 complex in Rhodobacter sphaeroides. Biochem J 298:197–205

    PubMed  CAS  Google Scholar 

  • Lang HP, Cogdell RJ, Takaichi S, Hunter CN (1995) Complete DNA sequence, specific Tn5 insertion map, and gene assignment of the carotenoid biosynthesis pathway of Rhodobacter sphaeroides. J Bacteriol 177:2064–2073

    PubMed  CAS  Google Scholar 

  • Liaaen-Jensen S, Cohen-Basire G, Nakayama TO, Stanier RY (1958) The path of carotenoid synthesis in a photosynthetic bacterium. Biochim Biophys Acta 29:447–498. doi:10.1016/0006-3002(58)90003-9

    Article  Google Scholar 

  • Malhorta HC, Britton G, Goodwin TW (1970) The occurrence of hydroxy-derivatives of phytoene and phytofluene in diphenylamine-inhibited cultures of Rhodospirillum rubrum. FEBS Lett 6:334–336. doi:10.1016/0014-5793(70)80091-6

    Article  Google Scholar 

  • McDermott G, Prince SM, Freer AA, Hawthornthwaite-Lawless AM, Papiz MZ, Cogdell RJ, Isaacs NW (1995) Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374:517–521. doi:10.1038/374517a0

    Article  CAS  Google Scholar 

  • Michalski WP, Nicolas DJD, Whatley FR (1985) Effects of nitrate, nitrite and diphenylamine on the photosynthetic apparatus of Rhodopseudomonas sphaeroides f. sp. denitrificans. J Gen Microbiol 131:1951–1961

    CAS  Google Scholar 

  • Moskalenko A, Erokhin YE (1974) Isolation of pigment–lipoprotein complexes from purple photosynthesizing bacteria by the method of preparative polyacryamide gel electrophoresis. Mikrobiologiia 43:654–658 (in Russian)

    PubMed  CAS  Google Scholar 

  • Moskalenko AA, Karapetyan NV (1996) Structural role of carotenoids in photosynthetic membranes. Z Naturforsch 51:763–771

    CAS  Google Scholar 

  • Moskalenko AA, Kuznetsova NY, Erokhin YE (1983) Isolation, spectral and photochemical properties of three types of pigment–protein complexes isolated from Chromatium with inhibited synthesis of carotenoids. Dokl Akad Nauk SSSR 269:1248–1251 (in Russian)

    CAS  Google Scholar 

  • Moskalenko AA, Britton G, Connor A, Young A, Toropygina O (1991) The carotenoid content in the chromatophores and pigment–protein complexes isolated from cells of Chromatium minutissimum. Biol Membr USSR 8:249–260

    CAS  Google Scholar 

  • Moskalenko A, Toropygina O, Makhneva ZK (1997) Behavior of carotenoids in Rhodospirillum rubrum cells under cultivation with diphenylamine. Dokl Akad Nauk 355:259–261 (in Russian)

    Google Scholar 

  • Moskalenko AA, Makhneva ZK, Fiedor L, Scheer H (2005) Effects of carotenoid inhibition on the photosynthetic RC–LH1 complex in purple sulphur bacterium Thiorhodospira sibirica. Photosynth Res 86:71–80. doi:10.1007/s11120-005-4473-9

    Article  PubMed  CAS  Google Scholar 

  • Papiz MZ, Prince SM, Howard T, Cogdell RJ, Isaacs NW (2003) The structure and thermal motion of the B800–850 LH2 complex from Rps. acidophila at 2.0 Å resolution and 100 K: new structural features and functionally relevant motions. J Mol Biol 326:1523–1538. doi:10.1016/S0022-2836(03)00024-X

    Article  PubMed  CAS  Google Scholar 

  • Prince SM, Howard TD, Myles DA, Wilkinson C, Papiz MZ, Freer AA, Cogdell RJ, Isaacs NW (2003) Detergent structure in crystals of the integral membrane light-harvesting complex LH2 from Rhodopseudomonas acidophila Strain 10050. J Mol Biol 326:307–315. doi:10.1016/S0022-2836(02)01361-X

    Article  PubMed  CAS  Google Scholar 

  • Renger G (2008) Primary process in photosynthesis part 1–2, principles and apparatus. In: Renger G (ed) Comprehensicve series in photochemical and photobiological sciences. RSC Publishing, Cambridge

    Google Scholar 

  • Schmidt K (1978) Biosynthesis of carotenoids. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum Press, New York, pp 729–750

    Google Scholar 

  • Schmidt K, Liaaen-Jensen S (1973) Bacterial carotenoids. XLII New keto-carotenoids from Rhodopseudomonas globiformis (Rhodospirilliaceae). Acta Chem Scand 27:3040–3052. doi:10.3891/acta.chem.scand.27-3040

    Article  PubMed  CAS  Google Scholar 

  • Schwerzmann RU, Bachofen R (1989) Carotenoid profile in pigment–protein complexes of Rhodospirillum rubrum. Plant Cell Physiol 30:497–504

    CAS  Google Scholar 

  • Takaichi S (1999) Carotenoids and carotenogenesis in anoxygenic photosynthetic bacteria. In: Frank HA, Young AJ, Britton G, Cogdell RJ (eds) The photochemistry of carotenoids. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 39–69

    Google Scholar 

  • Theiss C, Theiss , Leupold D, Moskalenko AA, Razjivin AD, Eichler HJ, Lokstein H (2008) Femtosecond transient absorption spectroscopy of native and carotenoid-less purple bacterial LH2 clarifies functions of carotenoids. Biophys J 94:4808–4811. doi:10.1529/biophysj.107.121681

    Article  PubMed  CAS  Google Scholar 

  • Zuber Z, Cogdell RJ (1995) Structure and organization of purple bacterial antenna complexes. In: Blakenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 315–348

    Google Scholar 

Download references

Acknowledgements

The project was supported by the Russian Foundation for Basic Research (06-04-48516 and 09-04-00522).

Author information

Authors and Affiliations

  1. Institute of Basic Biological Problems RAS, Pushchino, 142290, Russia

    Zoya Makhneva, Maksim Bolshakov & Andrey Moskalenko

Authors
  1. Zoya Makhneva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maksim Bolshakov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrey Moskalenko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrey Moskalenko.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Makhneva, Z., Bolshakov, M. & Moskalenko, A. Heterogeneity of carotenoid content and composition in LH2 of the purple sulphur bacterium Allochromatium minutissimum grown under carotenoid-biosynthesis inhibition. Photosynth Res 98, 633–641 (2008). https://doi.org/10.1007/s11120-008-9384-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-008-9384-0

Keywords

Search

Navigation