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Characterization of the chlorosome antenna of the filamentous anoxygenic phototrophic bacterium Chloronema sp. strain UdG9001

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Abstract

The absorption and fluorescence properties of chlorosomes of the filamentous anoxygenic phototrophic bacterium Chloronema sp. strain UdG9001 were analyzed. The chlorosome antenna of Chloronema consists of bacteriochlorophyll (BChl) d and BChl c together with γ-carotene as the main carotenoid. HPLC analysis combined with APCI LC-MS/MS showed that the chlorosomal BChls comprise a highly diverse array of homologues that differ in both the degree of alkylation of the macrocycle at C-8 and/or C-12 and the alcohol moiety esterified to the propionic acid group at C-17. BChl c and BChl d from Chloronema were mainly esterified with geranylgeraniol (33% of the total), heptadecanol (24%), octadecenol (19%), octadecanol (14%), and hexadecenol (9%). Despite this pigment heterogeneity, fluorescence emission of the chlorosomes showed a single peak centered at 765 nm upon excitation at wavelengths ranging from 710 to 740 nm. This single emission, assigned to BChl c, indicates an energy transfer from BChl d to BChl c within the same chlorosome. Likewise, incubation of chlorosomes under reducing conditions caused a weak increase in fluorescence emission, which indicates a small redox-dependent fluorescence. Finally, protein analysis of Chloronema chlorosomes using SDS-PAGE and MALDI-TOF-MS revealed the presence of a chlorosomal polypeptide with a molecular mass of 5.7 kDa, resembling the CsmA protein found in Chloroflexus aurantiacus and Chlorobium tepidum chlorosomes. Several minor polypeptides were also detected but not identified. These results indicate that, compared with other members of filamentous anoxygenic phototrophic bacteria and green sulfur bacteria, Chloronema possesses an antenna system with novel features that may be of interest for further investigations.

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Abbreviations

APCI LC-MS/MS :

Atmospheric pressure chemical ionization liquid chromatography mass spectrometry

BChl :

Bacteriochlorophyll

Chl.:

Chlorobium

Cfl.:

Chloroflexus

MALDI-TOF-MS :

Matrix assisted laser desorption/ionization time-of-flight mass spectrometry

[Et] :

Ethyl

[i-Bu] :

Isobutyl

[Me] :

Methyl

[neo-Pent] :

Neopentyl

[n-Pr] :

Propyl

t R :

Retention time

References

  • Airs RL, Keely BJ (2002) Atmospheric pressure chemical ionisation liquid chromatography/mass spectrometry of bacteriochlorophylls from Chlorobiaceae: characteristic fragmentations. Rapid Comm Mass Spectrom 16:453–461

    Article  CAS  Google Scholar 

  • Airs RL, Atkinson JE, Keely BJ (2001a) Development and application of a high resolution liquid chromatographic method for the analysis of complex pigment distributions. J Chromatogr A 917:169–179

    Article  Google Scholar 

  • Airs RL, Borrego CM, Garcia-Gil J, Keely BJ (2001b) Identification of the bacteriochlorophyll homologues of Chlorobium phaeobacteroides strain UdG6053 grown at low light intensity. Photosynth Res 70:221–229

    Google Scholar 

  • Arellano JB, Borrego CM, Martínez-Planells A, Garcia-Gil LJ (2001) Effect of carotenoid deficiency on cells and chlorosomes of Chlorobium phaeobacteroides. Arch Microbiol 175:226–233

    CAS  PubMed  Google Scholar 

  • Bañeras L, Borrego CM, Garcia-Gil LJ (1999) Growth-rate-dependent bacteriochlorophyll c/d ratio in the antenna of Chlorobium limicola strain UdG6040. Arch Microbiol 171:350–354

    Article  Google Scholar 

  • Borrego CM, Garcia-Gil LJ (1994) Separation of Bacteriochlorophyll homologs from green photosynthetic sulfur bacteria by reversed-phase HPLC. Photosynth Res 41:157–163

    CAS  Google Scholar 

  • Borrego CM, Garcia-Gil LJ (1995) Rearrangement of light harvesting bacteriochlorophyll homologs as a response of green sulfur bacteria to low light intensities. Photosynth Res 45:21–30

    CAS  Google Scholar 

  • Borrego CM, Garcia-Gil LJ, Cristina XP, Vila X, Abella CA (1998) Occurrence of new bacteriochlorophyll d forms in natural populations of green photoisynthetic sulfur bacteria. FEMS Microbiol Ecol 26:257–267

    Google Scholar 

  • Caple MB, Chow H, Strouse CE (1978) Photosynthetic pigments of green sulfur bacteria. The esterifying alcohols of bacteriochlorophylls c from Chlorobium limicola. J Biol Chem 253:6730–6737

    CAS  PubMed  Google Scholar 

  • Dubinina GA, Gorlenko VM (1975) New filamentous photosynthetic green bacteria containing gas vacuoles. Mikrobiologiya 44:511–517 (English translation) 44:452–458

  • Eichler B, Pfennig N (1990) Seasonal development of anoxygenic phototrophic bacteria in a holomictic drumlin lake (Schleinsee, F.R.G.). Arch Microbiol 119:369–392

    Google Scholar 

  • Eisen JA, Nelson KE, Paulsen IT, Heidelberg JF, Wu M, Dodson RJ, Deboy R, Gwinn ML, Nelson WC, Haft DH, Hickey EK, Peterson JD, Durkin AS, Kolonay JL, Yang F, Holt I, Umayam LA, Mason T, Brenner M, Shea TP, Parksey D, Feldblyum TV, Hansen CL, Craven MB, Radune D, Khouri H, Fujii CY, White O, Venter JC, Volfovsky N, Gruber TM, Ketchum KA, Tettelin H, Bryant DA, Fraser CM (2002) The complete genome sequence of the green sulfur bacterium Chlorobium tepidum. Proc Natl Acad Sci USA 99:9509–9514

    Article  CAS  PubMed  Google Scholar 

  • Elowitz MB, Levine AJ, Siggia ED, Swain PS (2002) Stochastic gene expression in a single cell. Science 297:1183–1186

    Article  CAS  PubMed  Google Scholar 

  • Fages F, Griebenow N, Griebenow K, Holzwarth AR, Schaffner K (1990) Characterization of light-harvesting pigments of Chloroflexus aurantiacus. Two new chlorophylls: oley (octadec-9-enyl) and cetyl (hexadecanyl) bacteriochlorophyllides-c. J Chem Soc Perkin Trans I: 2791–2797

    Google Scholar 

  • Feick RG, Fuller RC (1984) Topography of the photosynthetic apparatus of Chloroflexus aurantiacus. Biochemistry 23:3693–3700

    CAS  Google Scholar 

  • Feick R, Shiozawa JA, Ertlmaier A (1995) Biochemical and spectroscopic properties of the reaction center of the green filamentous bacterium Chloroflexus aurantiacus. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht, pp 699–708

  • Frigaard NU, Matsuura K, Hirota M, Miller M, Cox RP (1998) Studies on the location and function of isoprenoid quinones in chlorosomes from green sulfur bacteria. Photosynth Res 58:81–90

    Article  CAS  Google Scholar 

  • Gich F, Garcia-Gil LJ, Overmann J (2001a) Previously unknown and phylogenetically diverse members of the green nonsulfur bacteria are indigenous to freshwater lakes. Arch Microbiol 177:1–10

    Article  CAS  PubMed  Google Scholar 

  • Gich FB, Borrego CM, Martínez-Planells A, Steensgaard DB, Garcia-Gil LJ, Holzwarth AR (2001b) Variability of the photosynthetic antenna of a Pelodictyon clathratiforme population from a freshwater holomictic pond. FEMS Microbiol Ecol 37:11–19

    Article  CAS  Google Scholar 

  • Glaeser J, Bañeras L, Rütters H, Overmann J (2002) Novel bacteriochlorophyll e structures and species-specific variability of pigment composition in green sulfur bacteria. Arch Microbiol 177:475–485

    Article  CAS  PubMed  Google Scholar 

  • Gorlenko VM, Pierson BK (2001) The genus Chloronema. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology, vol. I, 2nd edn. Springer, Berlin Heidelberg New York, pp 437–438

  • Holzwarth AR, Schaffner K (1994) On the structure of bacteriochlorophyll molecular aggregates in the chlorosomes of green bacteria. A molecular modelling study. Photosynth Res 41:225–233

    CAS  Google Scholar 

  • Keppen OI, Baulina OI, Lysenko AM, Kondratieva EN (1993) New green bacterium belonging to the family Chloroflexaceae. Mikrobiologiya 62:267–274

    CAS  Google Scholar 

  • Keppen OI, Baulina OI, Kondratieva EN (1994) Oscillochloris trichoides neotype strain DG-6. Photosynth Res 41:29–33

    CAS  Google Scholar 

  • Kussmann M, Nordhoff E, Nielsen HR, Haebel S, Larsen MR, Jakobsen L, Gobom J, Mirgorodskay K, Kristensen AK, Palm L, Roepstorff P (1997) MALDI MS sample preparation techniques designed for various peptide and protein analytes. J Mass Spectrom 32:593–601

    CAS  Google Scholar 

  • Larsen KL, Miller M, Cox RP (1995) Incorporation of long-chain alcohols into bacteriochlorophyll c homologs by Chloroflexus aurantiacus. Arch Microbiol 163:119–123

    Article  CAS  Google Scholar 

  • Martínez-Planells A, Arellano JB, Borrego CM, López-Iglésias C, Gich F, Garcia-Gil LJ (2002) Determination of the topography and biometry of chlorosomes by atomic force microscopy. Photosynth Res 71:83–90

    Article  CAS  Google Scholar 

  • Niedermeier G, Shiozawa JA, Lottspeich F, Feick RG (1994) The primary structure of two chlorosome proteins from Chloroflexus aurantiacus . FEBS Lett. 342:61–65

  • Nozawa T, Ohtomo K, Suzuki M, Morishita Y, Madigan MT (1991a) Structures of bacteriochlorophyll c’s in chlorosomes from a new thermophilic bacterium Chlorobium tepidum. Chem Lett 1763–1766.

  • Nozawa T, Suzuki M, Ohtomo K, Morishita Y, Konami H, Madigan MT (1991b) Aggregation structure of bacteriochlorophyll c in chlorosomes from Chlorobium tepidum. Chem Lett 1641–1644.

  • Nozawa T, Ohtomo K, Takeshita N, Morishita Y, Osawa M, Madigan MT (1992) Substituents effects on the aggregation of bacteriochlorophyll d homologues purified from Chlorobium limicola. Bull Chem Soc Jpn 65:3493–3494

    CAS  Google Scholar 

  • Oelze J, Golecki JR (1995) Membranes and chlorosomes of Green Bacteria: Structure, composition and development. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht, pp 259–278

  • Otte SCM, van de Meent EJ, van Veelen PA, Pundsnes A, Amesz J (1993) Identification of the major chlorosomal bacteriochlorophylls of the green sulfur bacteria Chlorobium vibrioforme and Chlorobium phaeovibrioides; their functions in lateral energy transfer. Photosynth Res 35:159–169

    CAS  Google Scholar 

  • Overmann J, Tilzer MM (1989) Control of primary productivity and the significance of photosynthetic bacteria in a meromictic kettle lake, Mittlerer Buchensee, West-Germany. Aquatic Sciences 52:261–278

    Google Scholar 

  • Persson S, Sönksen CP, Frigaard NU, Cox RP, Roepstorff P, Miller M (2000) Pigments and proteins in green bacterial chlorosomes studied by matrix-assisted laser desorption ionization mass spectrometry. Eur J Biochem 267:450–456

    Article  CAS  PubMed  Google Scholar 

  • Pierson BK (2001) Filamentous Anoxygenic Phototrophic Bacteria. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology, vol. I, 2nd edn. Springer, Berlin Heidelberg New York, pp 427–429

  • Prokhorenko VI, Steensgaard DB, Holzwarth AR (2000) Exciton dynamics in the chlorosomal antennae of the green bacteria Chloroflexus aurantiacus and Chlorobium tepidum. Biophys J 79:2105–2120

    CAS  PubMed  Google Scholar 

  • Risch N, Brockmann JrH, Gloe A (1979) Structure of new bacteriochlorophylls from Chloroflexus aurantiacus. Liebigs Ann Chem, pp 408–418

  • Sakuragi Y, Frigaard N-U, Shimada K, Matsuura K (1999) Association of bacteriochlorophyll a with the CsmA protein in chlorosomes of the photosynthetic green filamentous bacterium Chloroflexus aurantiacus. Biochim et Biophys Acta 1413:172–180

    Article  CAS  Google Scholar 

  • Sauer K, Lindsay-Smith JR, Schultz AJ (1986) The dimerization of chlorophyll a, chlorophyll b, and bacteriochlorophyll in solution. J Am Chem Soc 88:2681–2688

    Google Scholar 

  • Schmidt K (1980) A comparative study on the composition of chlorosomes (Chlorobium vesicles) and cytoplasmic membranes from Chloroflexus aurantiacus strain Ok-70-fl and Chlorobium limicola f. thiosulfatophilum strain 6230. Arch Microbiol 124:21–31

    CAS  Google Scholar 

  • Senge MO, Smith KM (1995) Biosynthesis and structures of the bacteriochlorophylls. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht, pp 137–151

  • Smith KM, Bobe FW (1987) Light adaptation of bacteriochlorophyll-d producing bacteria by enzymic methylation of their antenna pigments. J Chem Soc Chem Comm 276–277

  • Stanier RY, Smith JHC (1960) The chlorophylls of green bacteria. Biochim Biophys Acta 41:478–484

    Article  CAS  PubMed  Google Scholar 

  • Steenbergen CLM, Korthals HJ, Baker AL, Watras CJ (1989) Microscale vertical distribution of algal and bacterial plankton in Lake Vechten (The Netherlands). FEMS Microbiol Ecol 62:209–220

    Article  Google Scholar 

  • Steensgaard DB, Cox RP, Miller M (1996) Manipulation of the bacteriochlorophyll c homolog distribution in the green sulfur bacterium Chlorobium tepidum. Photosynth Res 48:385–393

    CAS  Google Scholar 

  • Steensgaard DB, van Walree CA, Bañeras L, Borrego CM, Garcia-Gil LJ, Holzwarth AR (1999) Evidence for spatially separate bacteriochlorophyll c and bacteriochlorophyll d pools within the chlorosomal aggregate of the green sulfur bacterium Chlorobium limicola. Photosynth Res 59:231–241

    Article  CAS  Google Scholar 

  • Steensgaard DB, van Walree CA, Permentier H, Bañeras L, Borrego CM, Garcia-Gil LJ, Amesz J, Holzwarth A (2000a) Fast energy transfer between BChl d and BChl c in chlorosomes of the green sulfur bacterium Chlorobium limicola. Biochim Biophys Acta 1457:71–80

    Article  CAS  PubMed  Google Scholar 

  • Steensgaard DB, Wackerbarth H, Hildebrandt P, Holzwarth AR (2000b) Diastereoselective control of bacteriochlorophyll e aggregation. 31-S-BChl e is essential for the formation of chlorosome-like aggregates. J Phys Chem B 104:10379–10386

    Article  CAS  Google Scholar 

  • Theroux SJ, Redlinger TE, Fuller RC, Robinson SJ (1990) Gene encoding the 5.7-kilodalton chlorosome protein of Chloroflexus aurantiacus: regulated message levels and a predicted carboxy-terminal protein extension. J Bacteriol 172:4497–450

    CAS  PubMed  Google Scholar 

  • Trüper HG, Pfennig N (1992) The family Chlorobiaceae. In: Ballows A, Trüper HG, Dworkin M, Harden W, Schleifer KH (eds) The prokaryotes, 2nd edn. Springer, Berlin Heidelberg New York, pp 3583–3592

  • Vassilieva EV, Frigaard N-U, Bryant DA (2000) Chlorosomes: the light-harvesting complexes of the green bacteria. The Spectrum 13:7–13

    CAS  Google Scholar 

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Acknowledgements

This study was supported by The European Union through the TMR Program, Contract Nº FMRX-CT96–0081. F.B. Gich was the recipient of a Research Fellowship (1997FI-00738) from the Generalitat de Catalunya.

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Correspondence to Carles M. Borrego.

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Gich, F., Airs, R.L., Danielsen, M. et al. Characterization of the chlorosome antenna of the filamentous anoxygenic phototrophic bacterium Chloronema sp. strain UdG9001. Arch Microbiol 180, 417–426 (2003). https://doi.org/10.1007/s00203-003-0608-6

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