Bryan, Samantha J., Burroughs, Nigel John, Evered, Carol, Sacharz, Joanna, Nenninger, Anja, Mullineaux, Conrad W. and Spence, Edward M.. (2011) Loss of the SPHF homologue Slr1768 leads to a catastrophic failure in the maintenance of thylakoid membranes in synechocystis sp. PCC 6803. PLoS One, Vol.6 (No.5). e19625. ISSN 1932-6203

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Abstract

Background: In cyanobacteria the photosystems are localised to, and maintained in, specialist membranes called the thylakoids. The mechanism driving the biogenesis of the thylakoid membranes is still an open question, with only two potential biogenesis factors, Vipp1 and Alb3 currently identified. Methodology/Principal Findings: We generated a slr1768 knockout using the pGEM T-easy vector and REDIRECT. By comparing growth and pigment content (chlorophyll a fluoresence) of the Delta slr1768 mutant with the wild-type, we found that Dslr1768 has a conditional phenotype; specifically under high light conditions (130 mu mol m(-2) s(-1)) thylakoid biogenesis is disrupted leading to cell death on a scale of days. The thylakoids show considerable disruption, with loss of both structure and density, while chlorophyll a density decreases with the loss of thylakoids, although photosynthetic efficiency is unaffected. Under low light (30 mu mol m(-2) s(-1)) the phenotype is significantly reduced, with a growth rate similar to the wildtype and only a low frequency of cells with evident thylakoid disruption. Conclusions/Significance: This is the first example of a gene that affects the maintenance of the thylakoid membranes specifically under high light, and which displays a phenotype dependent on light intensity. Our results demonstrate that Slr1768 has a leading role in acclimatisation, linking light damage with maintenance of the thylakoids.

Item Type:	Journal Article
Subjects:	Q Science > QR Microbiology
Divisions:	Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010) Faculty of Science > Life Sciences (2010- ) Faculty of Science > Centre for Systems Biology Faculty of Science > Life Sciences (2010- ) > Warwick HRI (2004-2010)
Library of Congress Subject Headings (LCSH):	Cyanobacteria -- Physiology, Thylakoids, Chloroplasts -- Formation, Cyanobacteria -- Genetics, Bacterial cell walls
Journal or Publication Title:	PLoS One
Publisher:	Public Library of Science
ISSN:	1932-6203
Date:	23 May 2011
Volume:	Vol.6
Number:	No.5
Page Range:	e19625
Identification Number:	10.1371/journal.pone.0019625
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Open Access
Funder:	University of Warwick, Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC)
Grant number:	BB/G021856/1 (BBSRC)
References:	1. Stanier RY, Cohen-Bazire G (1977) Phototrophic prokaryotes: the cyanobacteria. Annu Rev Microbiol 31: 225–274. 2. Mullineaux CW (1999) The thylakoid membranes of cyanobacteria: structure, dynamics and function. . Aust J Plant Physiol 26: 671–677. 3. Srivastava R, Battchikova N, Norling B, Aro EM (2006) Plasma membrane of Synechocystis PCC 6803: a heterogeneous distribution of membrane proteins. Arch Microbiol 185: 238–243. 4. Nickelsen J, Rengstl B, Stengel A, Schottkowski M, Soll J, et al. (2011) Biogenesis of the cyanobacterial thylakoid membrane system--an update. FEMS Microbiol Lett 315: 1–5. 5. Hinterstoisser B, Cichna M, Kunter O, Peschek GA (1993) Cooperation of plasma and thylakoid membranes for the biosynthesis of chlorophyll in cyanobacteria: the role of thylakoid centres. J Plant Physiol 142: 407–413. 6. van de Meene AM, Hohmann-Marriott MF, Vermaas WF, Roberson RW (2006) The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803. Arch Microbiol 184: 259–270. 7. Zak E, Norling B, Maitra R, Huang F, Andersson B, et al. (2001) The initial steps of biogenesis of cyanobacterial photosystems occur in plasma membranes. Proc Natl Acad Sci U S A 98: 13443–13448. 8. Vothknecht UC, Westhoff P (2001) Biogenesis and origin of thylakoid membranes. Biochim Biophys Acta 1541: 91–101. 9. Westphal S, Heins L, Soll J, Vothknecht UC (2001) Vipp1 deletion mutant of Synechocystis: a connection between bacterial phage shock and thylakoid biogenesis? Proc Natl Acad Sci U S A 98: 4243–4248. 10. Sundberg E, Slagter JG, Fridborg I, Cleary SP, Robinson C, et al. (1997) ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria. Plant Cell 9: 717–730. 11. Kroll D, Meierhoff K, Bechtold N, Kinoshita M, Westphal S, et al. (2001) VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation. Proc Natl Acad Sci U S A 98: 4238–4242. 12. Srivastava R, Pisareva T, Norling B (2005) Proteomic studies of the thylakoid membrane of Synechocystis sp. PCC 6803. Proteomics 5: 4905–4916. 13. Aseeva E, Ossenbuhl F, Sippel C, Cho WK, Stein B, et al. (2007) Vipp1 is required for basic thylakoid membrane formation but not for the assembly of thylakoid protein complexes. Plant Physiol Biochem 45: 119–128. 14. Fuhrmann E, Gathmann S, Rupprecht E, Golecki J, Schneider D (2009) Thylakoid membrane reduction affects the photosystem stoichiometry in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 149: 735–744. 15. Bellafiore S, Ferris P, Naver H, Gohre V, Rochaix JD (2002) Loss of Albino3 leads to the specific depletion of the light-harvesting system. Plant Cell 14: 2303–2314. 16. Gerdes L, Bals T, Klostermann E, Karl M, Philippar K, et al. (2006) A second thylakoid membrane-localized Alb3/OxaI/YidC homologue is involved in proper chloroplast biogenesis in Arabidopsis thaliana. J Biol Chem 281: 16632–16642. 17. Ossenbuhl F, Gohre V, Meurer J, Krieger-Liszkay A, Rochaix JD, et al. (2004) Efficient assembly of photosystem II in Chlamydomonas reinhardtii requires Alb3.1p, a homolog of Arabidopsis ALBINO3. Plant Cell 16: 1790–1800. 18. Spence E, Bailey S, Nenninger A, Moller SG, Robinson C (2004) A homolog of Albino3/OxaI is essential for thylakoid biogenesis in the cyanobacterium Synechocystis sp. PCC6803. J Biol Chem 279: 55792–55800. 19. Ossenbuhl F, Inaba-Sulpice M, Meurer J, Soll J, Eichacker LA (2006) The Synechocystis sp PCC 6803 oxa1 homolog is essential for membrane integration of reaction center precursor protein pD1. Plant Cell 18: 2236–2246. 20. Merkwirth C, Langer T (2009) Prohibitin function within mitochondria: essential roles for cell proliferation and cristae morphogenesis. Biochim Biophys Acta 1793: 27–32. 21. Akiyama Y (2009) Quality control of cytoplasmic membrane proteins in Escherichia coli. J Biochem 146: 449–454. 22. Belfort M, Wulff DL (1973) Genetic and biochemical investigation of the Escherichia coli mutant hfl-1 which is lysogenized at high frequency by bacteriophage lambda. J Bacteriol 115: 299–306. 23. Gautsch JW, Wulff DL (1974) Fine structure mapping, complementation, and physiology of Escherichia coli hfl mutants. Genetics 77: 435–448. 24. van Bloois E, Dekker HL, Froderberg L, Houben EN, Urbanus ML, et al. (2008) Detection of cross-links between FtsH, YidC, HflK/C suggests a linked role for these proteins in quality control upon insertion of bacterial inner membrane proteins. FEBS Lett 582: 1419–1424. 25. Saikawa N, Akiyama Y, Ito K (2004) FtsH exists as an exceptionally large complex containing HflKC in the plasma membrane of Escherichia coli. J Struct Biol 146: 123–129. 26. Cheng HH, Muhlrad PJ, Hoyt MA, Echols H (1988) Cleavage of the cII protein of phage lambda by purified HflA protease: control of the switch between lysis and lysogeny. Proc Natl Acad Sci U S A 85: 7882–7886. 27. Gust B, Challis GL, Fowler K, Kieser T, Chater KF (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci U S A 100: 1541–1546. 28. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294: 2310–2314. 29. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. 30. Boehm M, Nield J, Zhang P, Aro EM, Komenda J, et al. (2009) Structural and mutational analysis of band 7 proteins in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 191: 6425–6435. 31. Hinderhofer M, Walker CA, Friemel A, Stuermer CA, Moller HM, et al. (2009) Evolution of prokaryotic SPFH proteins. BMC Evol Biol 9: 10. 32. Lemaire C, Hamel P, Velours J, Dujardin G (2000) Absence of the mitochondrial AAA protease Yme1p restores F0-ATPase subunit accumulation in an oxa1 deletion mutant of Saccharomyces cerevisiae. J Biol Chem 275: 23471–23475. 33. Browman DT, Hoegg MB, Robbins SM (2007) The SPFH domain-containing proteins: more than lipid raft markers. Trends Cell Biol 17: 394–402. 34. Rippka R, Josette Deruelles, John BWaterbury, Michael Herdman, Roger YStanier (1979) Generic Assignments, Strain Histories and Properties of Pure Cultures of Cyanobacteria. Journal of General Microbiology 111: 1–61. 35. Golden SS (1988) Mutagenesis of cyanobacteria by classical and gene-transferbased methods. Methods Enzymol 167: 714–727. 36. Gelman A, Rubin D B (1992) Inference from Iterative Simulation Using Multiple Sequences. Statistical Science 7: 457–472. 37. Gust B, Kieser T, Chater K (2002) PCR targeting system in Streptomyces coelicolor A3(2). John Innes Centre, Norwich Research Park, Colney, Norwich NR4 7UH, UK. 38. MacKinney G (1941) Absorption of light of chlorophyll solutions. J Biol Chem 140: 315–322. 39. Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26: 31–43.
URI:	http://wrap.warwick.ac.uk/id/eprint/39927

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