Ultrastructural analysis and identification of envelope proteins of "Candidatus chloracidobacterium thermophilum" chlorosomes

Journal of Bacteriology

Volumn 193, Issue 23, 2011, Pages 6701-6711

  Costas, Amaya M Garcia ^a,d   Tsukatani, Yusuke ^a,e   Romberger, Steven P ^a   Oostergetel, Gert T ^a   Boekema, Egbert J ^a   Golbeck, John H ^a,b   Bryant, Donald A ^a,c  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c MONTANA STATE UNIVERSITY   (United States)

^d MONTANA STATE UNIVERSITY BILLINGS   (United States)

^e RITSUMEIKAN UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CSMA PROTEIN; CSMR PROTEIN; CSMS PROTEIN; CSMT PROTEIN; CSMU PROTEIN; ENVELOPE PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (QUINONE); UNCLASSIFIED DRUG; BACTERIAL PROTEIN;

ARTICLE; BACTERIAL GROWTH; BACTERIUM ISOLATION; CHLORACIDOBACTERIUM THERMOPHILUM; CONTROLLED STUDY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PURIFICATION; ACIDOBACTERIA; AMINO ACID SEQUENCE; CELL ORGANELLE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; MOLECULAR WEIGHT; SEQUENCE ALIGNMENT; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ACIDOBACTERIA; BACTERIA (MICROORGANISMS); CHLOROBACULUM TEPIDUM; CHLOROBI; CHLOROFLEXI; CHLOROFLEXI (CLASS); THERMOPHILUM;

ACIDOBACTERIA; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; ORGANELLES; SEQUENCE ALIGNMENT;

EID: 84855396956     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.06124-11     Document Type: Article

References (72)

1. Blankenship, R. E., et al. 1993. Redox regulation of energy transfer efficiency in antennas of green photosynthetic bacteria. Photochem. Photobiol. 57:103-107.
2. Blankenship, R. E. 2002. Molecular mechanisms of photosynthesis. Blackwell Science Ltd., Oxford, England.
3. Blum, H., H. Beier, and H. Gross. 1987. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8:93-99.
4. Bryant, D. A., et al. 2011. Comparative and functional genomics of anoxygenic green bacteria from the taxa Chlorobi, Chloroflexi, and Acidobacteria, p. 47-102. In R. L. Burnap, and W. Vermaas (ed.), Advances in photosynthesis and respiration, vol. 33. Functional genomics and evolution of photosynthetic systems. Springer, Dordrecht, The Netherlands.
5. Bryant, D. A., et al. 2007. Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic acidobacterium. Science 317:523-526.
6. Bryant, D. A., and N.-U. Frigaard. 2006. Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol. 14:488-496.
7. 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.
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., 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.
10. Chung, S., G. Shen, J. Ormerod, and D. A. Bryant. 1998. Insertional inactivation studies of the csmA and csmC genes of the green sulfur bacterium Chlorobium vibrioforme 8327: the chlorosome protein CsmA is required for viability by CsmC is dispensible. FEMS Microbiol. Lett. 164:353-361.
11. Feick, R. G., and R. C. Fuller. 1984. Topography of the photosynthetic apparatus of Chloroflexus aurantiacus. Biochemistry 23:3693-3700.
12. Frangakis, A. S., and R. Hegerl. 2001. Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J. Struct. Biol. 135:239-250.
13. 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.
14. Frigaard, N.-U., K. Matsuura, M. Hirota, M. Miller, and R. P. Cox. 1998. Studies of the location and function of isoprenoid quinones in chlorosomes from green sulfur bacteria. Photosynth. Res. 58:181-190.
15. Frigaard, N.-U., S. Tokita, and K. Matsuura. 1999. Exogenous quinones inhibit photosynthetic electron transfer in Chloroflexus aurantiacus by specific quenching of the excited bacteriochlorophyll c antenna. Biochim. Biophys. Acta 1413:108-116.
16. 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.
17. 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.
18. 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.
19. Frigaard, N.-U., and D. A. Bryant. 2006. Chlorosomes: antenna organelles in photosynthetic green bacteria, p. 79-114. In J. M. Shively (ed.), Complex structures in prokaryotes, vol. 2. Springer, Berlin, Germany.
20. Ganapathy, S., et al. 2009. Alternating syn-anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes. Proc. Natl. Acad. Sci. U. S. A. 106:8525-8530.
21. Garcia Costas, A. M. 2010. Isolation and characterization of Candidatus Chloracidobacterium thermophilum. Ph.D. thesis.The Pennsylvania State University, University Park, PA.
22. Garcia Costas, A. M., et al. Complete genome of Candidatus Chloracidobacterium thermophilum, a chlorophyll-based photoheterotroph belonging to the phylum Acidobacteria. Environ. Microbiol., in press.
23. Gasteiger, E., et al. 2003. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31:3784-3788.
24. Gich, F., et al. 2003. Characterization of the chlorosome antenna of the filamentous anoxygenic phototrophic bacterium Chloronema sp. strain UdG9001. Arch. Microbiol. 180:417-426.
25. Gloe, A., and N. Risch. 1978. Bacteriochlorophyll cs, a new bacteriochlorophyll from Chloroflexus aurantiacus. Arch. Microbiol. 118:153-156.
26. Golbeck, J. H. 1993. Shared thematic elements in photochemical reaction centers. Proc. Natl. Acad. Sci. U. S. A. 90:1642-1646.
27. Gomez Maqueo Chew, A., and D. A. Bryant. 2007. Chlorophyll biosynthesis in bacteria: the origins of structural and functional diversity. Annu. Rev. Microbiol. 53:89-104.
28. Gomez Maqueo Chew, A., N.-U. Frigaard, and D. A. Bryant. 2007. Bacteriochlorophyllide c C-8(2) and C-12(1) methyltransferases are essential for adaptation to low light in Chlorobaculum tepidum. J. Bacteriol. 189:6176-6184.
29. Hohmann-Marriott, M. F., R. E. Blankenship, and R. W. Roberson. 2005. The ultrastructure of Chlorobium tepidum chlorosomes revealed by electron microscopy. Photosynth. Res. 86:145-154.
30. Klatt, C. G., et al. 2011. Metagenomic analyses of phototrophic hot spring microbial mat communities. ISME J. 5:1262-1278.
31. Kremer, J. R., D. N. Mastronarde, and J. R. McIntosh. 1996. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116:71-76.
32. Lanyi, J. K. 2006. Proton transfers in the bacteriorhodopsin photocycle. Biochim. Biophys. Acta 1757:1012-1018.
33. Larson, C. R., et al. 2011. The three-dimensional structure of the FMO protein from Pelodictyon phaeum and the implications for energy transfer. Photosynth. Res. 107:139-150.
34. 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, PA.
35. 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.
36. Li, H., and D. A. Bryant. 2009. Envelope proteins of the CsmB/CsmF and CsmC/CsmD motif families influence the size, shape, and composition of chlorosomes in Chlorobaculum tepidum. J. Bacteriol. 191:7109-7120.
37. Liu, Z., et al. 2011. Metatranscriptomic analyses of chlorophototrophs of a hot-spring microbial mat. ISME J. 5:1279-1290.
38. Madigan, M. T., S. R. Petersen, and T. D. Brock. 1974. Nutritional studies on Chloroflexus, a filamentous photosynthetic, gliding bacterium. Arch. Microbiol. 100:97-103.
39. Martinez-Planells, A., et al. 2002. Determination of the topography and biometry of chlorosomes by atomic force microscopy. Photosynth. Res. 71:83-90.
40. Masse, A. M., R. L. Airs, B. J. Keely, and R. de Wit. 2004. The impact of different intensities of green light on the bacteriochlorophyll homologue composition of the Chlorobiaceae: Prosthecochloris aestuarii and Chlorobium phaeobacteroides. Microbiology 150:2555-2564.
41. Montaño, G. A., et al. 2003. Characterization of Chlorobium tepidum chlorosomes: a calculation of bacteriochlorophyll c per chlorosome and oligomer modeling. Biophys. J. 85:2560-2565.
42. 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 42:10246-10451.
43. Ohnishi, T. 1998. Iron-sulfur clusters/semiquinones in complex 1. Biochim. Biophys. Acta 1364:186-206.
44. Olson, J. M. 2004. The FMO protein. Photosynth. Res. 80:181-187.
45. Oostergetel, G. T., et al. 2007. Long-range organization of bacteriochlorophyll in chlorosomes of Chlorobium tepidum investigated by cryo-electron microscopy. FEBS Lett. 581:5435-5439.
46. Pedersen, M. Ø., J. Borch, P. Højrup, R. P. Cox, and M. Miller. 2006. The light-harvesting antenna of Chlorobium tepidum: interactions between the FMO protein and the major chlorosome protein CsmA studied by surface plasmon resonance. Photosynth. Res. 89:63-69.
47. Pedersen, M. Ø., J. Linnanto, N.-U. Frigaard, N. C. Nielsen, and M. Miller. 2010. A model of the protein-pigment baseplate complex in chlorosomes of photosynthetic green bacteria. Photosynth. Res. 104:233-243.
48. Prokhorenko, V. I., D. B. Steensgaard, and A. R. Holzwarth. 2003. Exciton theory for supramolecular chlorosomal aggregates. 1. Aggregate size dependence of the linear spectra. Biophys. J. 85:3173-3186.
49. Pšenčík, J., Y. Z. Ma, J. B. Arellano, J. Hála, and T. Gillbro. 2003. Excitation energy transfer dynamics and excited-state structure in chlorosomes of Chlorobium phaeobacteroides. Biophys. J. 84:1161-1179.
50. Pšenčík, J., et al. 2004. Lamellar organization of pigments in chlorosomes, the light harvesting complexes of green photosynthetic bacteria. Biophys. J. 87:1165-1172.
51. Pšenčík, J., et al. 2006. Internal structure of chlorosomes from browncolored Chlorobium species and the role of carotenoids in their assembly. Biophys. J. 91:1433-1440.
52. Pšenčík, J., et al. 2009. Structure of chlorosomes from the green filamentous bacterium Chloroflexus aurantiacus. J. Bacteriol. 191:6701-6708.
53. Saga, Y., et al. 2002. Spectral heterogeneity in single light-harvesting chlorosomes from green sulfur photosynthetic bacterium Chlorobium tepidum. Photochem. Photobiol. 75:433-436.
54. Saga, Y., and H. Tamiaki. 2006. Transmission electron microscopic study on supramolecular nanostructures of bacteriochlorophyll self-aggregates in chlorosomes of green photosynthetic bacteria. J. Biosci. Bioeng. 102:118-123.
55. Schagger, H., and G. Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel eleoctrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
56. Shibata, Y., Y. Saga, H. Tamiaki, and S. Itoh. 2006. Low-temperature fluorescence from single chlorosomes, photosynthetic antenna complexes of green filamentous and sulfur bacteria. Biophys. J. 91:3787-3796.
57. Sprague, S. G., L. A. Staehelin, M. J. DiBartolomeis, and R. C. Fuller. 1981. Isolation and development of chlorosomes in the green bacterium Chloroflexus aurantiacus. J. Bacteriol. 147:1021-1031.
58. Staehelin, L. A., J. R. Golecki, R. C. Fuller, and G. Drews. 1978. Visualization of the supramolecular architecture of chlorosomes (Chlorobium type vesicles) in freeze-fractured cells of Chloroflexus aurantiacus. Arch. Microbiol. 119:269-277.
59. 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.
60. Tang, K.-H., et al. 2011. Complete genome sequence of the filamentous anoxygenic phototrophic bacterium Chloroflexus aurantiacus. BMC Genomics 12:334.
61. 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.
62. Tronrud, D. E., J. Wen, L. Gay, and R. E. Blankenship. 2009. The structural basis for the difference in absorbance spectra for the FMO antenna protein from various green sulfur bacteria. Photosynth. Res. 100:79-87.
63. Tsukatani, Y., J. Wen, R. E. Blankenship, and D. A. Bryant. 2010. Characterization of the bacteriochlorophyll a-binding, Fenna-Matthews-Olson protein from Candidatus Chloracidobacterium thermophilum. Photosynth. Res. 104:201-209.
64. van de Meene, A. M., T. Le Olson, A. M. Collins, and R. E. Blankenship. 2007. Initial characterization of the photosynthetic apparatus of "Candidatus Chlorothrix halophila," a filamentous, anoxygenic photoautotroph. J. Bacteriol. 189:4196-4203.
65. van Dorssen, R. J., P. D. Gerola, J. M. Olson, and J. Amesz. 1986. Optical and structural properties of chlorosomes of the photosynthetic green sulfur bacterium Chlorobium limicola. Biochim. Biophys. Acta 848:77-82.
66. Vassilieva, E. V., et al. 2001. Electron transfer may occur in the chlorosome envelope: the CsmI and CsmJ proteins of chlorosomes are 2Fe-2S ferredoxins. Biochemistry 40:464-473.
67. Vassilieva, E. V., et al. 2002. Subcellular localization of chlorosome proteins in Chlorobium tepidum and characterization of three new chlorosome proteins: CsmF, CsmH and CsmX. Biochemistry 41:4358-4370.
68. Wang, J., D. C. Brune, and R. E. Blankenship. 1990. Effects of oxidants and reductants on the efficiency of excitation transfer in green photosynthetic bacteria. Biochim. Biophys. Acta 1015:457-463.
69. Wen, J., et al. 2011. Structural and spectroscopic insights of the FMO antenna protein of the aerobic chlorophototroph Candidatus Chloracidobacterium thermophilum. Biochim. Biophys. Acta 1807:157-164.
70. Wen, J., H. Zhang, M. L. Gross, and R. E. Blankenship. 2009. Membrane orientation of the FMO antenna protein from Chlorobaculum tepidum as determined by mass spectrometry-based footprinting. Proc. Natl. Acad. Sci. U. S. A. 106:6134-6139.
71. Wen, J., H. Zhang, M. L. Gross, and R. E. Blankenship. 2011. Native electrospray mass spectrometry reveals the nature and stoichiometry of pigments in the FMO photosynthetic antenna protein. Biochemistry 50:3502-3511.
72. Zhou, W., R. LoBrutto, S. Lin, and R. E. Blankenship. 1994. Redox effects on the bacteriochlorophyll a-containing Fenna-Matthews-Olson protein from Chlorobium tepidum. Photosynth. Res. 41:89-96.