Abstract
Bioenergetics of a primordial cyanobacterium Gloeobacter violaceus PCC 7421 were discussed based on genome information and experimental results. Absence of thylakoid membranes in this species induced inevitable coupling of the two electron transfer systems, i.e. photosynthesis and respiration, on cytoplasmic membranes by sharing common components. There were multiple pathways for a respiratory electron transfer system, and they affected the redox state of quinone molecules in the pool through the redox equilibrium among components. Even though experimental analysis on this species was not abundant, a principal point of the energetics is now becoming clear. In addition, a whole genome analysis and comparative genomics brought about many important informations on the components for photosynthesis, respiration, metabolism, and regulation. In many cases, this species lacks genes related to bioenergetics, however malfunction of the system was not necessarily observed, indicating presence of an alternative way to establish reaction systems found in other cyanobacterial species. By a combination of the two kinds of information, we discussed the bioenergetics in the unique species, G. violaceus.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Béjà O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP, Jovanovich SB, Gates CM, Feldman RA, Spudich JL, Spudich EN and DeLong EF (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289: 1902–1906
Berry S, Schneider D, Vermaas WFJ and Rögner M (2002) Electron transport route in whole cells of Synechocystis sp. strain PCC 6803: the route of the cytochrome bd-type oxidase. Biochemistry 41: 3422–3429
Blankenship RE (2001) Molecular evidences for evolution of photosynthesis. Trends Plant Sci 6: 4–6
Bryant DA, Cohen-Bazire G and Glazer AN (1981) Characterization of the biliproteins of Gloeobacter violaceus. Chromophore content of a cyanobacterial phycoerythrin carrying phycourobilin chromophore. Arch Microbiol 129: 190–198
De Las Rivas J and Barber J (2004) Analysis of the structure of the PsbO protein and its implications. Photosynth Res 81: 329–343
Ferreira K, Iverson T, Maghlaoui K, Barber J and Iwata S (2004) Architecture of the photosynthetic oxygen-evolving canter. Science 303: 1831–1838
Frankenberg N, Mukougawa K, Kohchi T and Lagarias JC (2001) Functional genomic analysis of the HY2 family of ferredoxin-dependent bilin reductases from oxygenic photosynthetic organisms. Plant Cell 13: 965–978
Gantt E (1981) Phycobilisomes. Annu Rev Plant Physiol 32: 327–347
Guglielmi G, Cohen-Bazire G and Bryant DA (1981) The structure of Gloeobacter violaceus and its phycobilisomes. Arch Microbiol 129: 181–189
Güler S, Seeliger A, Härtel H, Renger G and Benning C (1996) A null mutant of Synechococcus sp. PCC7942 deficient in the sulfolipid sulfoquinovosyl diacylglycerol. J Biol Chem 271: 7501–7507
Guo H and Xu X (2004) Broad host range plasmid-based gene transfer system in the cyanobacterium Gloeobacter violaceus which lacks thylakoids. Prog Natl Sci 14: 31–35
Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni M and Saenger W (2009) Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Bio 16: 334–342
Gutiérrez-Cirlos EB, Pérez-Gómez B, Krogmann DW and Gómez-Lojerob C (2006) The phycocyanin-associated rod linker proteins of the phycobilisome of Gloeobacter violaceus PCC 7421 contain unusually located rod-capping domains. Biochim Biophys Acta 1757: 130–134
Hiratsuka T, Furihata K, Ishikawa J, Yamashita H, Itoh N, Seto H and Dairi T (2008) An alternative menaquinone biosynthetic pathway operating in microorganisms. Science 321: 1670–1673
Huynen MA, Dandekar T and Bork P (1999) Variation and evolution of the citric-acid cycle: a genomic perspective. Trends Microbiol 7: 281–291
Inoue H, Tsuchiya T, Satoh S, Miyashita H, Kaneko T, Tabata S, Tanaka A and Mimuro M (2004) Unique constitution of photosystem I with a novel subunit in the cyanobacterium Gloeobacter violaceus PCC 7421. FEBS Lett 578: 275–279
Kamiya N and Shen J-R (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7 Å resolution. Proc Natl Acad Sci U S A 100: 98–103
Kato Y, Nakamura A, Suzawa T and Watanabe T (2008) In Allen J, Gantt E, Golbeck J and Osmond B (eds) Photosynthesis Energy from the Sun, Springer, New York 109–112
Koenig F and Schmidt M (1995) Gloeobacter violaceus-investigation of an unusual photosynthetic apparatus, absence of the long wavelength emission of photosystem I in 77 K fluorescence spectra. Physiol Plant 94: 621–628
Kondo K, Geng XX, Katayama M and Ikeuchi M (2005) Distinct roles of CpcG1 and CpcG2 in phycobilisome assembly in the cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res 84: 269–273
Koyama K, Tsuchiya T, Akimoto S, Yokono M, Miyashita H and Mimuro M (2006) New linker proteins in phycobilisomes isolated from the cyanobacterium Gloeobacter violaceus PCC 7421. FEBS Lett 580: 3457–3461
Koyama K, Suzuki H, Noguchi T, Akimoto S, Tsuchiya T and Mimuro M (2008) Oxygen evolution activities in the thylakoid-lacking cyanobacterium Gloeobacter violaceus PCC 7421. Biochim Biophys Acta 1777: 369–378
Krogmann DW, Pérez-Gómez B, Gutiérrez-Cirlos EB, Chagolla-López A, de la Vara LG and Gómez-Lojero C (2007) The presence of multidomain linkers determines the bundle-shape structure of the phycobilisome of the cyanobacterium Gloeobacter violaceus PCC 7421. Photosynth Res 93: 27–43
Kroll D, Meierhoff K, Bechtold N, Kinoshita M, Westphal S, Vothknecht UC, Soll J and Westhoff P (2001) VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation. Proc Nat Acad Sci U S A 98: 4238–4242
Loll B, Kern J, Saenger W, Zouni A and Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosysterm II. Nature 438: 1040–1044
McDonald AE and Vanlerberghe GC (2006) Origins, evolutionary history, and taxonomic distribution of alternative oxidase and plastoquinol terminal oxidase. Comparative Biochem Physiol, Part D 1: 357–364
Mangels D, Kruip J, Berry S, Rögner M, Boekema EJ and Koenig F (2002) Photosystem I from the unusual cyanobacterium Gloeobacter violaceus. Photosynth Res 72: 307–319
Mimuro M, Lipschultz CA and Gantt E (1986) Energy flow in the phycobilisome core of Nostoc sp. (MAC): two independent terminal pigments. Biochim Biophys Acta 852: 126–132
Mimuro M, Ookubo T, Takahashi D, Sakawa T, Akimoto S, Yamazaki I and Miyashita H (2002) Unique fluorescence properties of a cyanobacterium Gloeobacter violaceus PCC 7421: reasons for absence of the long-wavelength PSI Chl a fluorescence at –196°C. Plant Cell Physiol 43: 587–594
Mimuro M, Tsuchiya T, Inoue H, Sakuragi Y, Itoh Y, Gotoh T, Miyashita H, Bryant DA and Kobayashi M (2005) The secondary electron acceptor of photosystem I in Gloeobacter violaceus PCC 7421 is menaquinone-4 that is synthesized by a unique but unknown pathway. FEBS Lett 579: 3493–3496
Mimuro M, Tomo T and Tsuchiya T (2008a) Two unique cyanobacteria lead to a new view on the appearance of oxygenic photosynthesis. Photosynth Res 97: 167–176
Mimuro M, Kobayashi M, Murakami A, Tsuchiya T and Miyashita H (2008b) Structure and function of antenna systems: oxygen evolving cyanobacteria. In Renger G (ed) Primary Processes of Photosynthesis: Basic Principles and Apparatus, Part 1, pp 261–299. RSC Publishing, Cambridge
Miranda MRM, Choi AR, Shi L, Bezerra Jr AG, Jung K-H and Brown LS (2009) The photocycle and proton translocation pathway in a cyanobacterial ion-pumping rhodopsin. Biophys J 96: 1471–1481
Mogi T and Miyoshi H (2009) Properties of cytochrome bd plastoquinol oxidase from the cyanobacterium Synechocystis sp. PCC 6803. J Biochem 145: 395–401
Motoki A, Usui M, Shimazu T, Hirano M and Katoh S (2002) A domain of the manganese stabilizing protein from Synechococcus elongatus involved in functional binding to photosystem II. J Biol Chem 277: 14747–14756
Nakamura Y, Kaneko T, Sato S, Mimuro M, Miyashita H, Tsuchiya T, Sasamoto S, Watanabe A, Kawashima K, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Nakazaki N, Shimpo S, Takeuchi C, Yamada M and Tabata S (2003) Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. DNA Res 10: 137–145
Nelissen B, Van de Peer Y, Wilmotte A and De Wachter R (1995) An early origin of plastids within the cyanobacterial divergence is suggested by evolutionary trees based on complete 16S rRNA sequences. Mol Biol Evol 12: 1166–1173
Olson JM and Blankenship RE (2004) Thinking about the evolution of photosynthesis. Photosynth Res 80: 373–386
Paumann M, Regelsberger G, Obinger C and Peschek GA (2005) The bioenergetic role of dioxygen and the terminal oxidase(s) in cyanobacteria. Biochim Biophys Acta 1707: 231–253
Peschek GA (2008) Electron transport chains in oxygenic cyanobacteria. In Renger G (ed) Primary Processes of Photosynthesis: Principles and Applications, pp 383–415. RSC Publishing, Cambridge
Rippka R, Waterbury J and Cohen-Bazire G (1974) A cyanobacterium which lacks thylakoids. Arch Microbiol 100: 419–436
Scheer H and Zhao KH (2008) Biliprotein maturation: the chromophore attachment. Mol Microbiol 68: 263–276
Selstam E and Campbell D (1996) Membrane lipid composition of the unusual cyanobacterium Gloeobacter violaceus sp. PCC 7421, which lacks sulfoquinovosyl diacylglycerol. Arch Microbiol 166: 132–135
Schmetterer G (1994) Cyanobacterial respiration. The Molecular Biology of Cyanobacteria, pp 409–435. Kluwer Academic, Dordrecht
Sicora CI, Brown CM, Cheregi O, Vass I and Campbell DA (2008) The psbA gene family responds differentially to light and UVB stress in Gloeobacter violaceus PCC 7421, a deeply divergent cyanobacterium. Biochim Biophys Acta 1777: 130–139
Sobotka R, Dühring U, Komenda J, Peter E, Gardian Z, Tichy M, Grimm B and Wilde A (2008) Importance of the cyanobacterial Gun4 protein for chlorophyll metabolism and assembly of photosynthetic complexes. J Biol Chem 283: 25794–25802
Steiger S, Jackisch Y and Sandmann G (2005) Carotenoid biosynthesis in Gloeobacter violaceus PCC4721 involves a single crtI-type phytoene desaturase instead of typical cyanobacterial enzymes. Arch Microbiol 184: 207–214
Tsuchiya T, Takaichi S, Misawa N, Maoka T, Miyashita H and Mimuro M (2005) The cyanobacterium Gloeobacter violaceus PCC 7421 uses bacterial-type phytoene desaturase in carotenoid biosynthesis. FEBS Lett 579: 2125–2129
Westphal S, Heins L, Soll J and Vothknecht UC (2001) Vipp1 deletion mutant of Synechocystis: A connection between bacterial phage shock and thylakoid biogenesis? Proc Nat Acad Sci U S A 98: 4243–4248
Yano J, Kern J, Sauer K, Latimer MJ, Pushkar Y, Biesiadka J, Loll B, Saenger W, Messinger J, Zouni A and Yachandra VK (2006) Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster. Science 314: 821–825
Yano J and Yachandra VK (2008) Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster from X-ray spectroscopy. Inorg Chem 47: 1711–1726
Yokono M, Akimoto S, Koyama K, Tsuchiya T and Mimuro M (2008) Energy transfer processes in Gloeobacter violaceus PCC 7421 that possesses phycobilisomes with a unique morphology. Biochim Biophys Acta 1777: 55–65
Zhang CC, Jeanjean R and Joset F (1998) Obligate phototrophy in cyanobacteria: more than a lack of sugar transport. FEMS Microbio Lett 161: 285–292
Acknowledgments
The authors would like to express sincere thanks to Prof. G. A. Peschek, University of Vienna, for his giving us a chance to write this article. This work was supported in part by the Grant-in-Aids for the Creative Research from the Japanese Society for Promotion of Science (JSPS) to MM (Grant No. 17GS0314). We also thank Mr. H. Inoue for his work in the early stage of our experiments.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Science+Business Media B.V.
About this chapter
Cite this chapter
Mimuro, M., Tsuchiya, T., Koyama, K., Peschek, G.A. (2011). Bioenergetics in a Primordial Cyanobacterium Gloeobacter violaceus PCC 7421. In: Peschek, G., Obinger, C., Renger, G. (eds) Bioenergetic Processes of Cyanobacteria. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0388-9_9
Download citation
DOI: https://doi.org/10.1007/978-94-007-0388-9_9
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-0352-0
Online ISBN: 978-94-007-0388-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)