Envelope proteins of the CsmB/CsmF and CsmC/CsmD motif families influence the size, shape, and composition of chlorosomes in Chlorobaculum tepidum

Journal of Bacteriology

Volumn 191, Issue 22, 2009, Pages 7109-7120

  Li, Hui ^a,b   Bryant, Donald A ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF WASHINGTON MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIOCHLOROPHYLL; BACTERIOCHLOROPHYLL C; PROTEIN CSMB; PROTEIN CSMC; PROTEIN CSMD; PROTEIN CSMF; UNCLASSIFIED DRUG;

ARTICLE; CHLOROBACULUM TEPIDUM; CHLOROBIACEAE; CHLOROSOME; CONTROLLED STUDY; GROWTH RATE; LIGHT ABSORPTION; LIGHT HARVESTING SYSTEM; LIGHT INTENSITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; WILD TYPE;

BACTERIAL PROTEINS; CHLOROBIUM; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTROPHORESIS, POLYACRYLAMIDE GEL; IMMUNOBLOTTING; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION;

CHLOROBACULUM TEPIDUM;

EID: 70449574690     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00707-09     Document Type: Article

References (53)

1. Blankenship, R. E. 1992. Origin and early evolution of photosynthesis. Photosynth. Res. 33:91-111.
2. Bryant, D. A., and N.-U. Frigaard. 2006. Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol. 14:488-496.
3. Bryant, D. A., A. M. Garcia Costas, J. A. Maresca, A. Gomez Maqueo Chew, C. G. Klatt, M. M. Bateson, L. J. Tallon, J. Hostetler, W. C. Nelson, J. F. Heidelberg, and D. M. Ward. 2007. "Candidatus Chloracidobacterium thermophilum": an aerobic phototrophic acidobacterium. Science 317:523-526.
4. Bryant, D. A., E. V. Vassilieva, N.-U. Frigaard, and H. Li. 2002. Selective protein extraction from Chlorobium tepidum chlorosomes using detergents. Evidence that CsmA forms multimers and binds bacteriochlorophyll a. Biochemistry 41:14403-14411.
5. Chung, S. 1995. Characterization of chlorosomes in green sulfur bacteria. Ph.D. dissertation. The Pennsylvania State University, University Park.
6. Chung, S., and D. A. Bryant. 1996. Characterization of csmB genes, encoding a 7.5-kDa protein of the chlorosome envelope, from the green sulfur bacteria Chlorobium vibrioforme 8327d and Chlorobium tepidum. Arch. Microbiol. 166:234-244. (Pubitemid 26352988)
7. Chung, S., and D. A. Bryant. 1996. Characterization of the csmD and csmE genes from Chlorobium tepidum. The CsmA, CsmC, CsmD, and CsmE proteins are components of the chlorosome envelope. Photosynth. Res. 50:41-59.
8. Chung, S., G. Frank, H. Zuber, and D. A. Bryant. 1994. Genes encoding two chlorosome components from the green sulfur bacteria Chlorobium vibrioforme strain 8327d and Chlorobium tepidum. Photosynth. Res. 41:261-275.
9. Chung, S., G. Shen, J. Ormerod, and D. A. Bryant. 1998. Insertional inactivation studies of csmA and csmC genes of the green sulfur bacterium Chlorobium vibrioforme 8327d: the chlorosome protein CsmA is required for viability but CsmC is dispensible. FEMS Microbiol. Lett. 164:353-361.
10. Dunphy, P. J., and A. F. Brodie. 1971. The structure and function of quinones in respiratory metabolism. Methods Enzymol. 18:407-461.
11. Feick, R. G., and R. C. Fuller. 1984. Topography of the photosynthetic apparatus of Chloroflexus aurantiacus. Biochemistry 23:3693-3700.
12. Frigaard, N.-U., and D. A. Bryant. 2001. Chromosomal gene inactivation in the green sulfur bacterium Chlorobium tepidum by natural transformation. Appl. Environ. Microbiol. 67:2538-2544.
13. Frigaard, N.-U., and D. A. Bryant. 2006. Chlorosomes: antenna organelles in green photosynthetic bacteria, p. 79-144. In J. M. Shively (ed.), Microbiology monographs, vol.2. Complex intracellular structures in prokaryotes. Springer, Berlin, Germany.
14. Frigaard, N.-U., H. Li, K. J. Milks, and D. A. Bryant. 2004. Nine mutants of Chlorobium tepidum each unable to synthesize a different chlorosome protein still assemble functional chlorosomes. J. Bacteriol. 186:646-653.
15. Frigaard, N.-U., H. Li, P. Martinsson, S. K. Das, H. A. Frank, T. J. Aartsma, and D. A. Bryant. 2005. Isolation and characterization of carotenosomes from a bacteriochlorophyll c-less mutant of Chlorobium tepidum. Photosynth. Res. 86:101-111. (Pubitemid 41361264)
16. Frigaard, N.-U., J. A. Maresca, C. E. Yunker, A. D. Jones, and D. A. Bryant. 2004. Genetic manipulation of carotenoid biosynthesis in the green sulfur bacterium Chlorobium tepidum. J. Bacteriol. 186:5210-5220.
17. Frigaard, N.-U., Y. Sakuragi, and D. A. Bryant. 2004. Gene inactivation in the cyanobacterium Synechococcus sp. PCC 7002 and the green sulfur bacterium Chlorobium tepidum using in vitro-made DNA constructs and natural transformation. Methods Mol. Biol. 274:325-340.
18. Frigaard, N.-U., S. Takaichi, M. Hirota, K. Shimada, and K. Matsuura. 1997. Quinones in chlorosomes of green sulfur bacteria and their role in the redox-dependent fluorescence studied in chlorosome-like bacteriochlorophyll c aggregates. Arch. Microbiol. 167:343-349.
19. Frigaard, N.-U., E. V. Vassilieva, H. Li, K. J. Milks, J. Zhao, and D. A. Bryant. 2001. The remarkable chlorosome. In PS2001 proceedings. Proc. 12th Int. Congr. Photosynth., article S1-003. CSIRO Publishing, Canberra, Australia.
20. Frigaard, N.-U., G. D. Voigt, and D. A. Bryant. 2002. Chlorobium tepidum mutant lacking bacteriochlorophyll c made by inactivation of the bchK gene, encoding bacteriochlorophyll c synthase. J. Bacteriol. 184:3368-3376.
21. Frydman, B., and H. Rappaport. 1963. Non-chlorophyllous pigments of Chlorobium thiosulfatophilum - chlorobiumquinone. J. Am. Chem. Soc. 85:823-825.
22. Ganapathy, S., G. T. Oostergetel, P. K. Wawrzyniak, M. Reus, A. Gomez Maqueo Chew, F. Buda, E. J. Boekema, D. A. Bryant, A. R. Holzwarth, and H. J. M. de Groot. 2009. Alternating syn-anti bacteriochlorophylls form supramolecular helical nanotubes in chlorosomes. Proc. Natl. Acad. Sci. USA 106:8525-8530.
23. 1 methyltransferases are essential for adaptation to low light in Chlorobaculum tepidum. J. Bacteriol. 189:6176-6184.
24. Holo, H., M. Broch-Due, and J. G. Ormerod. 1985. Glycolipids and the structure of chlorosomes in green bacteria. Arch. Microbiol. 143:94-99.
25. Ikonen, T. P., H. Li, J. Psencík, P. A. Laurinmäki, S. J. Butcher, N.-U. Frigaard, R. E. Serimaa, D. A. Bryant, and R. Tuma. 2007. X-ray scattering and electron cryomicroscopy study on the effect of carotenoid biosynthesis to the structure of Chlorobium tepidum chlorosomes. Biophys. J. 93:620-628.
26. Lehmann, R. P., R. A. Brunisholz, and H. Zuber. 1994. Structural differences in chlorosomes from Chloroflexus aurantiacus grown under different conditions support the BChl c-binding function of the 5.7 kDa polypeptide. FEBS Lett. 342:319-324.
27. Li, H. 2006. Organization and function of chlorosome proteins in the green sulfur bacterium Chlorobium tepidum. Ph.D. thesis. The Pennsylvania State University, University Park.
28. Li, H., N.-U. Frigaard, and D. A. Bryant. 2006. Molecular contacts for chlorosome envelope proteins revealed by cross-linking studies with chlorosomes from Chlorobium tepidum. Biochemistry 45:9095-9103. (Pubitemid 44156372)
29. Martinez-Planells, A., J. B. Arellano, C. M. Borrego, C. López-Iglesias, F. Gich, and J. Garcia-Gil. 2002. Determination of the topography and biometry of chlorosomes by atomic force microscopy. Photosynth. Res. 71:83-90.
30. Montaño, G. A., B. P. Bowen, J. T. LaBelle, N. W. Woodbury, V. B. Pizziconi, and R. E. Blankenship. 2003. Characterization of Chlorobium tepidum chlorosomes: a calculation of bacteriochlorophyll c per chlorosome and oligomer modeling. Biophys. J. 85:2560-2565.
31. Montaño, G. A., H. M. Wu, S. Lin, D. C. Brune, and R. E. Blankenship. 2003. Isolation and characterization of the B798 light-harvesting baseplate from the chlorosomes of Chloroflexus aurantiacus. Biochemistry 42:10246-10251.
32. Niedermeier, G., J. A. Shiozawa, F. Lottspeich, and R. G. Feick. 1994. The primary structure of two chlorosome proteins from Chloroflexus aurantiacus. FEBS Lett. 342:61-65.
33. Oelze, J. 1985. Analysis of bacteriochlorophylls. Methods Microbiol. 18:57-284.
34. Oostergetel, G. T., M. Reus, A. Gomez Maqueo Chew, D. A. Bryant, E. J. Boekema, and A. R. Holzwarth. 2007. Long-range organization of bacteriochlorophyll in chlorosomes of Chlorobium tepidum investigated by cryoelectron microscopy. FEBS Lett. 581:5435-5439.
35. Pedersen, M. Ø., L. Pham, D. B. Steensgaard, and M. Miller. 2008. A reconstituted light-harvesting complex from the green sulfur bacterium Chlorobium tepidum containing CsmA and bacteriochlorophyll a. Biochemistry 47:1435-1441.
36. Pedersen, M. Ø., J. Underhaug, J. Dittmer, M. Miller, and N. C. Nielsen. 2008. The three-dimensional structure of CsmA: a small antenna protein from the green sulfur bacterium Chlorobium tepidum. FEBS Lett. 582:2869-2874.
37. Psencík, J., J. B. Arellano, T. P. Ikonen, C. M. Borrego, P. A. Laurinmäki, S. J. Butcher, R. E. Serimaa, and R. Tuma. 2006. Internal structure of chlorosomes from brown-colored Chlorobium species and the role of carotenoids in their assembly. Biophys. J. 91:1433-1440.
38. Psencík, J., T. P. Ikonen, P. Laurinmäki, M. C. Merckel, S. J. Butcher, R. E. Serimaa, and R. Tuma. 2004. Lamellar organization of pigments in chlorosomes: the light harvesting complexes of green photosynthetic bacteria. Biophys. J. 87:1165-1172. (Pubitemid 39095093)
39. Saga, Y., Y. Shibata, S. Itoh, and H. Tamiaki. 2007. Direct counting of submicrometer-sized photosynthetic apparatus dispersed in medium at cryogenic temperature by confocal laser fluorescence microscopy: estimation of the number of bacteriochlorophyll c in single light-harvesting antenna complexes chlorosomes of green photosynthetic bacteria. J. Phys. Chem. B 111:12605-12609.
40. Sakuragi, Y., N.-U. Frigaard, K. Shimada, and K. Matsuura. 1999. Association of bacteriochlorophyll a with the CsmA protein in chlorosomes of the photosynthetic green filamentous bacterium Chloroflexus aurantiacus. Biochim. Biophys. Acta 1413:172-180. (Pubitemid 29507556)
41. Schägger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
42. Staehelin, L. A., J. R. Golecki, and G. Drews. 1980. Supramolecular organization of chlorosomes (Chlorobium vesicles) and of their membrane attachment sites in Chlorobium limicola. Biochim. Biophys. Acta 589:30-45.
43. Stanier, R. Y., and J. H. Smith. 1960. The chlorophylls of green bacteria. Biochim. Biophys. Acta 41:478-484.
44. Tang, K. H., J. Wen, X. Li, and R. E. Blankenship. 2009. Role of the AcsF protein in Chloroflexus aurantiacus. J. Bacteriol. 191:3580-3587.
45. Theroux, S. J., T. E. Redlinger, R. C. Fuller, and S. J. Robinson. 1990. Gene encoding the 5.7-kilodalton chlorosome protein of Chloroflexus aurantiacus: regulated message levels and a predicted carboxy-terminal protein extension. J. Bacteriol. 172:4497-4504.
46. Tsuji, K., S. Takaichi, K. Matsuura, and K. Shimada. 1995. Specificity of carotenoids in chlorosomes of the green filamentous bacterium, Chloroflexus aurantiacus, p. 99-103. In P. Mathis (ed.), Photosynthesis: from light to biosphere, vol.3. Kluwer, Dordrecht, The Netherlands.
47. Vassilieva, E. V., M. L. Antonkine, B. L. Zybailov, F. Yang, C. U. Jakobs, J. H. Golbeck, and D. A. Bryant. 2001. Electron transfer may occur in the chlorosome envelope: the CsmI and CsmJ proteins of chlorosomes are 2Fe-2S ferredoxins. Biochemistry 40:464-473.
48. Vassilieva, E. V., N.-U. Frigaard, and D. A. Bryant. 2000. Chlorosomes: the light-harvesting complexes of the green bacteria. Spectrum 13:7-13.
49. Vassilieva, E. V., J. G. Ormerod, and D. A. Bryant. 2002. Biosynthesis of chlorosome proteins is not inhibited in acetylene-treated cultures of Chlorobium vibrioforme. Photosynth. Res. 71:69-81.
50. Vassilieva, E. V., V. L. Stirewalt, C. U. Jakobs, N.-U. Frigaard, K. Inoue-Sakamoto, M. A. Baker, A. Sotak, and D. A. Bryant. 2002. Subcellular localization of chlorosome proteins in Chlorobium tepidum and characterization of three new chlorosome proteins: CsmF, CsmH, and CsmX. Biochemistry 41:4358-4370.
51. Wahlund, T. M., and M. T. Madigan. 1995. Genetic transfer by conjugation in the thermophilic green sulfur bacterium Chlorobium tepidum. J. Bacteriol. 177:2583-2588.
52. Wahlund, T. M., C. R. Woese, R. W. Castenholz, and M. T. Madigan. 1991. A thermophilic green sulfur bacterium from New Zealand hot springs, Chlorobium tepidum sp. nov. Arch. Microbiol. 156:81-90.
53. Wullink, W., J. Knudsen, J. M. Olson, T. E. Redlinger, and E. F. J. van Bruggen. 1991. Localization of polypeptides in isolated chlorosomes from green phototrophic bacteria by immuno-gold labeling electron microscopy. Biochim. Biophys. Acta 1060:97-105.