Skip to main content

Lipid Biosynthesis and its Regulation in Cyanobacteria

  • Chapter
Book cover Lipids in Photosynthesis

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 30))

Summary

According to the endosymbiosis theory, cyanobacteria are assumed to be ancestors of chloroplasts. They are Gram-negative and perform oxygenic photosynthesis via two photosystems, which resemble the photosystems in the chloroplasts of eukaryotic plants. The membranes of cyanobacteria contain four main glycerolipids, three of which are glycolipids, namely, monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DGDG), and sulfoquinovosyldiacylglycerol (SQDG), and one of which is the phospholipid phosphatidylglycerol (PG). The lipid composition of cyanobacterial membranes is similar to that of chloroplast membranes, and, in particular, to that of thylakoid membranes, and it is different from that of the membranes of most bacteria, which contain phospholipids as the major glyc-erolipids. The fatty acid composition of the membrane lipids of cyanobacteria differs among strains, and cyanobacteria can be classified into four groups in terms of their fatty acids. Among unsaturated fatty acids, monounsaturated to tetraunsaturated fatty acids have been found in cyanobacteria. In a limited number of cyanobacteria, the fatty acid composition resembles that of chloroplast membranes. The biosynthesis of membrane lipids in cyanobacteria has been studied in vivo by tracer experiments with radio-labeled compounds since the 1980s. However, the characterization and molecular identification of the enzymes involved in the biosynthesis of lipids had to await the cloning of the genes for these enzymes since most of these enzymes are membrane-bound and, thus, their solubilization and subsequent purification are relatively difficult. Genes for the desaturases of cyanobacteria, which introduce double bonds into fatty acids bound to membrane lipids, were cloned in the early 1990s, after identification of the desA gene that was able to complement a mutation that resulted in a defect in desaturation at the Δ12 position. Many genes for enzymes involved in the biosynthesis of various lipid classes were identified in the 2000s with the help of newly available databases of cyanobacterial genomic sequences. Many of the proteins encoded by the identified genes are homologous to their respective counterparts in chloro-plasts, supporting the endosymbiosis theory, but some of them are structurally distinct. This distinction suggests the possibility that original genes were replaced by unrelated genes during the evolution of chloroplasts from cyanobacteria. The biosynthesis of membrane lipids in cyanobacteria is regulated by environmental conditions, indicating that membrane lipids play an active role in adaptive processes. Studies of cyanobacterial lipids have shed light both on the evolution of chloroplasts and the adaptation of photosynthetic organisms to changes in environmental conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

ACP:

Acyl-carrier protein

CDP:

Cytidine 5'-diphosphate

CMP:

Cytidine 5'-monophosphate

CTP:

Cytidine 5'-triphosphate

Cyt b 5 :

Cytochrome b 5

DG:

Diacylglycerol

DGDG:

Digalactosyldiacylglycerol

ER:

Endoplasmic reticulum

FAS:

Fatty acid synthase

Fd:

Ferredoxin

FNR:

NADPH: ferredoxin oxidoreductase

GOGAT:

Glutamine: 2-oxoglutarate aminotransferase (glutamate synthase)

G3P:

Glycerol 3-phosphate

GPAT:

Glycerol-3-phosphate acyltransferase

LPA:

Lysophosphatidic acid

LPAAT:

Lysophosphatidic acid acyltransferase

MGDG:

Monogalactosyldiacylglycerol

MGlcDG:

Monoglucosyldiacylglycerol

ORF:

Open reading frame

PA:

Phosphatidic acid

PG:

Phosphatidylglycerol

PGP:

Phosphatidylglycerophosphate

PS:

Photosystem

SQDG:

Sulfoquinovosyldiacylglycerol

UDP:

Uridine 5'-diphosphate

X:Y:

A fatty acid with X carbon atoms and Y double bonds. Where indicated, numbers in parenthesis represent the positions of double bonds relative to the carboxyl end of the hydrocarbon chain

References

  • Aoki M, Sato N-R, Meguro A and Tsuzuki M (2004) Differing involvement of sulfoquinovosyl diacylglycerol in photosystem II in two species of unicellular cyanobacte-ria. Eur J Biochem 271: 685–693

    Article  PubMed  CAS  Google Scholar 

  • Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kap-itonov VV, Kröger N, Lau WW, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP and Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudo-nana: ecology, evolution, and metabolism. Science 306: 79–86

    Article  PubMed  CAS  Google Scholar 

  • Awai K, Kakimoto T, Awai C, Kaneko T, Nakamura Y, Taka-miya K, Wada H and Ohta H (2006) Comparative genomic analysis revealed a gene for monoglucosyldiacylglycerol synthase, an enzyme for photosynthetic membrane lipid synthesis in cyanobacteria. Plant Physiol 141: 1120–1127

    Article  PubMed  CAS  Google Scholar 

  • Awai K, Watanabe H, Benning C and Nishida I (2007) Diga-lactosyldiacylglycerol is required for better photosynthetic growth of Synechocystis sp. PCC 6803 under phosphate limitation. Plant Cell Physiol 48: 1517–1523

    Article  PubMed  CAS  Google Scholar 

  • Babiychuk E, Müller F, Eubel H, Braun HP, Frentzen M and Kushnir S (2003) Arabidopsis phosphatidylglycerophos-phate synthase 1 is essential for chloroplast differentiation, but is dispensable for mitochondrial function. Plant J 33: 899–909

    Article  PubMed  CAS  Google Scholar 

  • Behrouzian B and Buist PH (2003) Mechanism of fatty acid desaturation: a bioorganic perspective. Prostaglandins Leukot Essent Fatty Acids 68: 107–112

    Article  PubMed  CAS  Google Scholar 

  • Benning C (1998) Biosynthesis and function of the sulfo-lipid sulfoquinovosyl diacylglycerol. Annu Rev Plant Physiol Plant Mol Biol 49: 53–75

    Article  PubMed  CAS  Google Scholar 

  • Benning C, Beatty JT, Prince RC and Somerville CR (1993) The sulfolipid sulfoquinovosyldiacylglycerol is not required for photosynthetic electron transport in Rhodo-bacter sphaeroides but enhances growth under phosphate limitation. Proc Natl Acad Sci USA 90: 1561–1565

    Article  PubMed  CAS  Google Scholar 

  • Benning C, Huang ZH and Gage DA (1995) Accumulation of a novel glycolipid and a betaine lipid in cells of Rho-dobacter sphaeroides grown under phosphate limitation. Arch Biochem Biophys 317: 103–111

    Article  PubMed  CAS  Google Scholar 

  • Benson AA (1963) The plant sulfolipid. Adv Lipid Res 1: 387–394

    PubMed  CAS  Google Scholar 

  • Benson AA and Maruo B (1958) Plant phospholipids. I. Identification of the phosphatidyl glycerols. Biochim Bio-phys Acta 27: 189–195

    Article  CAS  Google Scholar 

  • Browse J and Somerville C (1991) Glycerolipid synthesis: biochemistry and regulation. Annu Rev Plant Physiol Plant Mol Biol 42: 467–506

    Article  CAS  Google Scholar 

  • Cai YP and Wolk CP (1990) Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120 to select for double recombinants and to entrap insertion sequences. J Bacte-riol 172: 3138–3145

    CAS  Google Scholar 

  • Carter HE, McCluer RH and Slifer ED (1956) Lipids of wheat flour. I. Characterization of galactosylglycerol components. J Am Chem Soc 78: 3735–3738

    Article  CAS  Google Scholar 

  • Chintalapati S, Prakash JSS, Gupta P, Ohtani S, Suzuki I, Sakamoto T, Murata N and Shivaji S (2006) A novel Δ9 acyl-lipid desaturase, DesC2, from cyanobacteria acts on fatty acids esterified to the sn-2 position of glycerolipids. Biochem J 398: 207–214

    Article  PubMed  CAS  Google Scholar 

  • Chintalapati S, Prakash JSS, Singh AK, Ohtani S, Suzuki I, Murata N and Shivaji S (2007) Desaturase genes in a psy-chrotolerant Nostoc sp. are constitutively expressed at low temperature. Biochem Biophys Res Commun 362: 81–87

    Article  PubMed  CAS  Google Scholar 

  • Dörmann P, Balbo I and Benning C (1999) Arabidopsis galactolipid biosynthesis and lipid trafficking mediated by DGD1. Science 284: 2181–2184

    Article  PubMed  Google Scholar 

  • Dorne A-J, Joyard J and Douce R (1990) Do thylakoids really contain phosphatidylcholine? Proc Natl Acad Sci USA 87: 71–74

    Article  PubMed  CAS  Google Scholar 

  • Douglas SE and Turner S (1991) Molecular evidence for the origin of plasmids from a cyanobacterium-like ancestor. J Mol Evol 33: 267–273

    Article  PubMed  CAS  Google Scholar 

  • Dowhan W (1997) Molecular basis for membrane phospho-lipid diversity: why are there so many lipids? Annu Rev Biochem 66: 199–232

    Article  PubMed  CAS  Google Scholar 

  • Essigmann B, Güler S, Narang RA, Linke D and Benning C (1998) Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 95: 1950–1955

    Article  PubMed  CAS  Google Scholar 

  • Falcone DL, Gibson S, Lemieux B and Somerville C (1994) Identification of a gene that complements an Arabidop-sis mutant deficient in chloroplast ω6 desaturase activity. Plant Physiol 106: 1453–1459

    Article  PubMed  CAS  Google Scholar 

  • Froehlich JE, Poorman R, Reardon E, Barnum SR and Jaworski JG (1990) Purification and characterization of acyl carrier protein from two cyanobacteria species. Eur J Biochem 193: 817–825

    Article  PubMed  CAS  Google Scholar 

  • Giroud C, Geber A and Eichenberger W (1988) Lipids of Chlamydomonas reinhardtii. Analysis of molecular species and intracellular site(s) of biosynthesis. Plant Cell Physiol 29: 587–595

    CAS  Google Scholar 

  • Golden SS (1988) Mutagenesis of cyanobacteria by classical and gene-transfer-based methods. Methods Enzymol 167: 714–727

    Article  PubMed  CAS  Google Scholar 

  • Güler S, Seeliger A, Härtel H, Renger G and Benning C (1996) A null mutant of Synechococcus sp. PCC 7942 deficient in the sulfolipid sulfoquinovosyl diacylglycerol. J Biol Chem 271: 7501–7507

    Article  PubMed  Google Scholar 

  • Güler S, Essigmann B and Benning C (2000) A cyanobac-terial gene, sqdX, required for biosynthesis of the sul-folipid sulfoquinovosyldiacylglycerol. J Bacteriol 182: 543–545

    Article  PubMed  Google Scholar 

  • Gurr MI (1971) The biosynthesis of polyunsaturated fatty acids in plants. Lipids 6: 266–273

    Article  CAS  Google Scholar 

  • Hagio M, Gombos Z, Varkonyi Z, Masamoto K, Sato N-R, Tsuzuki M and Wada H (2000) Direct evidence for requirement of phosphatidylglycerol in photosystem II of photosynthesis. Plant Physiol 124: 795–804

    Article  PubMed  CAS  Google Scholar 

  • Hagio M, Sakurai I, Sato S, Kato T, Tabata S and Wada H (2002) Phosphatidylglycerol is essential for the development of thylakoid membranes in Arabidopsis thaliana. Plant Cell Physiol 43: 1456–1464

    Article  PubMed  CAS  Google Scholar 

  • Härtel H, Dörmann P and Benning C (2000) DGD1-independent biosynthesis of extraplastidic galactolipids after phosphate deprivation in Arabidopsis. Proc Natl Acad Sci USA 97: 10649–10654

    Article  PubMed  Google Scholar 

  • Heilmann I, Pidkowich MS, Girke T and Shanklin J (2004) Switching desaturase enzyme specificity by alternate sub-cellular targeting. Proc Natl Acad Sci USA 101: 10266– 10271

    Article  PubMed  CAS  Google Scholar 

  • Heinz E, Schmidt H, Hoch M, Jung KH, Binder H and Schmidt RR (1989) Synthesis of different nucleoside 5′-diphospho-sulfoquinovoses and their use for studies on sulfolipid biosynthesis in chloroplasts. Eur J Biochem 184: 445–453

    Article  PubMed  CAS  Google Scholar 

  • Higashi S and Murata N (1993) An in vivo study of substrate specificities of acyl-lipid desaturases and acyltransferases in lipid synthesis in Synechocystis PCC 6803. Plant Phys-iol 102: 1275–1278

    CAS  Google Scholar 

  • Inaba M, Suzuki I, Szalontai B, Kanesaki Y, Los DA, Hayashi H and Murata N (2003) Gene-engineered rigidi-fication of membrane lipids enhances the cold inducibility of gene expression in Synechocystis. J Biol Chem 278: 12191–12198

    Article  PubMed  CAS  Google Scholar 

  • Jürgen UJ and Benz R (1988) Pore-forming activity of outer membrane extracts from the unicellular cyanobacterium Synechocystis sp. PCC 6714. Z Naturforsch 44c: 165–169

    Google Scholar 

  • Kawarabayasi Y, Hino Y, Horikawa H, Jin-no K, Takahashi M, Sekine M, Baba S, Ankai A, Kosugi H, Hosoyama A, Fukui S, Nagai Y, Nishijima K, Otsuka R, Nakazawa H, Takamiya M, Kato Y, Yoshizawa T, Tanaka T, Kudoh Y, Yamazaki J, Kushida N, Oguchi A, Aoki K, Masuda S, Yanagii M, Nishimura M, Yamagishi A, Oshima T and Kikuchi H (2001) Complete genome sequence of an aerobic thermoacidophilic crenarchaeon, Sulfolobus tokodaii strain 7. DNA Res 8: 123–140

    Article  PubMed  CAS  Google Scholar 

  • Kearns EV, Hugly S and Somerville CR (1991) The role of cytochrome b 5 in Δ12 desaturation of oleic acid by microsomes of safflower (Carthamus tinctorius L.). Arch Biochem Biophys 284: 431–436

    Article  PubMed  CAS  Google Scholar 

  • Kelly AA and Dörmann P (2002) DGD2, an Arabidopsis gene encoding a UDP-galactose-dependent digalactos-yldiacylglycerol synthase, is expressed during growth under phosphate-limiting conditions. J Biol Chem 277: 1166–1173

    Article  PubMed  CAS  Google Scholar 

  • Kenyon CN (1972) Fatty acid composition of unicellular strains of blue-green algae. J Bacteriol 109: 827–834

    PubMed  CAS  Google Scholar 

  • Kenyon CN, Rippka R and Stanier RY (1972) Fatty acid composition and physiological properties of some filamentous blue-green algae. Arch Mikrobiol 83: 216–236

    Article  PubMed  CAS  Google Scholar 

  • Kiseleva LL, Serebriiskaya TS, Horvàth I, Vigh L, Lyuke-vich AA and Los DA (2000) Expression of the gene for the Δ9 acyl-lipid desaturase in the thermophilic cyanobac-terium. J Mol Microbiol Biotechnol 2: 331–338

    PubMed  CAS  Google Scholar 

  • Koyama K, Suzuki H, Noguchi T, Seiji Akimoto S, Tsuchiya T and Mimuro M (2008) Oxygen evolution in the thylakoid-lacking cyanobacterium Gloeobacter violaceus PCC 7421. Biochim Biophys Acta 1777: 369–378

    Article  PubMed  CAS  Google Scholar 

  • Laudenbach DE and Grossman A (1991) Characterization and mutagenesis of sulfur-regulated genes in a cyanobac-terium: evidence for function in sulfate transport. J Bacte-riol 173: 2739–2750

    CAS  Google Scholar 

  • Lem NW and Stumpf PK (1984a) In vitro fatty acid synthesis and complex lipid metabolism in the cyanobacterium Anabaena variabilis. I. Some characteristics of fatty acid synthesis. Plant Physiol 74: 134–138

    Article  CAS  Google Scholar 

  • Lem NW and Stumpf PK (1984b) In vitro fatty acid synthesis and complex lipid metabolism in the cyanobacterium Anabaena variabilis. II. Acyl transfer and complex lipid formation. Plant Physiol 75: 700–704

    Article  CAS  Google Scholar 

  • Li R and Watanabe MM (2001) Fatty acid profiles and their chemotaxonomy in planktonic species of Anabaena (cyanobacteria) with straight trichomes. Phytochemistry 57: 727–731

    Article  PubMed  CAS  Google Scholar 

  • Lindqvist Y, Huang W, Schneider G and Shanklin J (1996) Crystal structure of Δ9 stearoyl-acyl carrier protein desaturase from castor seed and its relationship to other di-iron proteins. EMBO J 15: 4081–4092

    PubMed  CAS  Google Scholar 

  • Liu X-J, Chen F and Jiang Y (2003) Differentiation of Nos-toc flagelliforme and its neighboring species using fatty-acid profiling as a chemotaxonomic tool. Curr Microbiol 47: 467–474

    Article  PubMed  CAS  Google Scholar 

  • Los DA and Murata N (1998) Structure and expression of fatty acid desaturases. Biochim Biophys Acta 1394: 3–15

    Article  PubMed  CAS  Google Scholar 

  • Los DA, Ray MK and Murata N (1997) Differences in the control of the temperature-dependent expression of four genes for desaturases in Synechocystis sp. PCC 6803. Mol Microbiol 25: 1167–1175

    Article  PubMed  CAS  Google Scholar 

  • Matsuzaki M, Misumi O, Shin-i T, Maruyama S, Takahara M, Miyagishima SY, Mori T, Nishida K, Yagisawa F, Nishida K, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta F, Nishizaka S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y, Asakawa S, Takano H, Ohta N, Kuroiwa H, Tanaka K, Shimizu N, Sugano S, Sato N, Nozaki H, Ogasawara N, Kohara Y and Kuroiwa T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidi-oschyzon merolae 10D. Nature 428: 653–657

    Article  PubMed  CAS  Google Scholar 

  • McKeon TA and Stumpf PK (1982) Purification and characterization of the stearoyl-acyl carrier protein desaturase and the acyl-acyl carrier protein thioesterase from maturing seeds of safflower. J Biol Chem 257: 12141–12147

    PubMed  CAS  Google Scholar 

  • Minoda A, Sato N-R, Nozaki H, Okada K, Takahashi H, Sonoike K and Tsuzuki M (2002) Role of sulfoquinovosyl diacylglyc-erol for the maintenance of photosystem II in Chlamydomonas reinhardtii. Eur J Biochem 269: 2353–2358

    Article  PubMed  CAS  Google Scholar 

  • Minoda A, Sonoike K, Okada K, Sato N-R and Tsuzuki M (2003) Decrease in the efficiency of the electron donation to tyrosine Z of photosystem II in an SQDG-deficient mutant of Chlamydomonas. FEBS Lett 553: 109–112

    Article  PubMed  CAS  Google Scholar 

  • Mizuno T, Kaneko T and Tabata S (1996) Compilation of all genes encoding bacterial two-component signal transducers in the genome of the cyanobacterium, Synechocystis sp. strain PCC 6803. DNA Res 3: 407–414

    Article  PubMed  CAS  Google Scholar 

  • Moche M, Dehesh K, Edwards P and Lindqvist Y (2001) The crystal structure of β-ketoacyl-acyl carrier protein synthase II from Synechocystis sp. at 1.54 Å resolution and its relationship to other condensing enzymes. J Mol Biol 305: 491–503

    Article  PubMed  CAS  Google Scholar 

  • Murata N and Los DA (2006) Histidine kinase Hik33 is an important participant in cold-signal transduction in cyano-bacteria. Physiol Plant 126: 17–27

    Article  CAS  Google Scholar 

  • Murata N and Suzuki I (2006) Exploitation of genomic sequences in a systematic analysis to access how cyanobac-teria sense environmental stress. J Exp Bot 57: 235–247

    Article  PubMed  CAS  Google Scholar 

  • Murata N and Wada H (1995) Acyl-lipid desaturases and their importance in the tolerance and acclimatization to cold of cyanobacteria. Biochem J 308: 1–8

    PubMed  CAS  Google Scholar 

  • Murata N, Wada H and Gombos Z (1992) Modes of fatty-acid desaturation in cyanobacteria. Plant Cell Physiol 33: 933–941

    CAS  Google Scholar 

  • 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 thyla-koids. DNA Res 10: 137–145

    Article  PubMed  CAS  Google Scholar 

  • Nakamura Y, Tsuchiya M and Ohta H (2007) Plastidic phos-phatidic acid phosphatases identified in a distinct subfamily of lipid phosphate phosphatases with prokaryotic origin. J Biol Chem 282: 29013–29021

    Article  PubMed  CAS  Google Scholar 

  • Napier JA, Sayanova O, Sperling P and Heinz E (1999) A growing family of cytochrome b 5-fusion proteins. Trends Plant Sci 4: 2–5

    Article  Google Scholar 

  • Nishida I and Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47: 541–568

    Article  PubMed  CAS  Google Scholar 

  • Nishiyama T, Fujita T, Shin IT, Seki M, Nishide H, Uchi-yama I, Kamiya A, Carninci P, Hayashizaki Y, Shinozaki K, Kohara Y and Hasebe M (2003) Comparative genomics of Physcomitrella patens gametophytic transcriptome and Arabidopsis thaliana: implication for land plant evolution. Proc Natl Acad Sci USA 100: 8007–8012

    Article  PubMed  CAS  Google Scholar 

  • Ohlrogge J and Browse J (1995) Lipid biosynthesis. Plant Cell 7: 957–970

    PubMed  CAS  Google Scholar 

  • Okazaki K, Sato N-R, Tsuji N, Tsuzuki M and Nishida I (2006) The significance of C16 fatty acids in the sn-2 position of glycerolipids in the photosynthetic growth of Synechocystis sp. PCC 6803. Plant Physiol 141: 546–556

    Article  PubMed  CAS  Google Scholar 

  • Quoc KP and Dubacq J-P (1997) Effect of growth temperature on the biosynthesis of eukaryotic lipid molecular species by the cyanobacterium Spirulina platensis. Biochim Biophys Acta 1346: 237–246

    Article  PubMed  CAS  Google Scholar 

  • Reddy AS, Nuccio ML, Gross LM and Thomas TL (1993) Isolation of a Δ6-desaturase gene from the cyanobacterium Synechocystis sp. strain PCC 6803 by gain-of-function expression in Anabaena sp. strain PCC 7120. Plant Mol Biol 27: 293–300

    Article  Google Scholar 

  • Riekhof WR, Ruckle ME, Lydic TA, Sears BB and Benning C (2003) The sulfolipids 2′-O-acyl-sulfoquinovosyldia-cylglycerol and sulfoquinovosyldiacylglycerol are absent from a Chlamydomonas reinhardtii mutant deleted in SQD1. Plant Physiol 133: 864–874

    Article  PubMed  CAS  Google Scholar 

  • Riekhof WR, Sears BB and Benning C (2005) Annotation of genes involved in glycerolipid biosynthesis in Chlamydomonas reinhardtii: discovery of the betaine lipid synthase BTA1Cr. Eukaryot Cell 4: 242–252

    Article  PubMed  CAS  Google Scholar 

  • Rippka R, Waterbury J and Cohen-Bazire G (1974) A cyanobacterium which lacks thylakoids. Arch Micro-biol 100: 419–436

    Article  CAS  Google Scholar 

  • Sakamoto T, Los DA, Higashi S, Wada H, Nishida I, Ohmori M and Murata N (1994a) Cloning of ω3 desaturase from cyanobacteria and its use in altering the degree of membrane-lipid unsaturation. Plant Mol Biol 26: 249–263

    Article  CAS  Google Scholar 

  • Sakamoto T, Wada H, Nishida I, Ohmori M and Murata N (1994b) Δ9 acyl-lipid desaturases of cyanobacteria. Molecular cloning and substrate specificities in terms of fatty acids, sn-positions, and polar head groups. J Biol Chem 269: 25576–25580

    CAS  Google Scholar 

  • Sakurai I, Shen JR, Leng J, Ohashi S, Kobayashi M and Wada H (2006) Lipids in oxygen-evolving photosystem II complexes of cyanobacteria and higher plants. J Biochem (Tokyo) 140: 201–209

    Article  CAS  Google Scholar 

  • Sakurai I, Mizusawa N, Wada H and Sato N-K (2007) Diga-lactosyldiacylglycerol is required for stabilization of the oxygen-evolving complex in photosystem II. Plant Phys-iol 145: 1361–1370

    Article  CAS  Google Scholar 

  • Sanda S, Leustek T, Theisen MJ, Garavito RM and Benning C (2001) Recombinant Arabidopsis SQD1 converts UDP-glu-cose and sulfite to the sulfolipid head group precursor UDP-sulfoquinovose in vitro. J Biol Chem 276: 3941–3946

    Article  PubMed  CAS  Google Scholar 

  • Sato N-K and Murata N (1982a) Lipid biosynthesis in the blue-green alga, Anabaena variabilis. I. Lipid classes. Biochim Biophys Acta 710: 271–278

    Article  CAS  Google Scholar 

  • Sato N-K and Murata N (1982b) Lipid biosynthesis in the bluegreen alga, Anabaena variabilis. II. Fatty acids and lipid molecular species. Biochim Biophys Acta 710: 279–289

    Article  CAS  Google Scholar 

  • Sato N-K and Murata N (1982c) Lipid biosynthesis in the blue-green alga (cyanobacterium), Anabaena variabi-lis. III. UDP-glucose: diacylglycerol glucosyltransferase activity in vitro. Plant Cell Physiol 23: 1115–1120

    CAS  Google Scholar 

  • Sato N-K, Murata N, Miura Y and Ueta N (1979) Effect of growth temperature on lipid and fatty acid compositions in the blue-green algae, Anabaena variabilis and Ana-cystis nidulans. Biochim Biophys Acta 572: 19–28

    Article  PubMed  CAS  Google Scholar 

  • Sato N-R (2004) Roles of the acidic lipids sulfoquinovosyl diacylglycerol and phosphatidylglycerol in photosynthesis: their specificity and evolution. J Plant Res 117: 495–505

    Article  PubMed  CAS  Google Scholar 

  • Sato N-R, Sonoike K, Tsuzuki M and Kawaguchi A (1995a) Impaired photosystem II in a mutant of Chlamydomonas reinhardtii defective in sulfoquinovosyl diacylglycerol. Eur J Biochem 234: 16–23

    Article  CAS  Google Scholar 

  • Sato N-R, Tsuzuki M, Matsuda M, Ehara T, Osafune T and Kawaguchi A (1995b) Isolation and characterization of mutants affected in lipid metabolism of Chlamydomonas reinhardtii. Eur J Biochem 230: 987–993

    Article  CAS  Google Scholar 

  • Sato N-R, Fujiwara S, Kawaguchi A and Tsuzuki M (1997) Cloning of a gene for chloroplast ω6 desaturase of a green alga, Chlamydomonas reinhardtii. J Biochem (Tokyo) 122: 1224–1232

    Article  CAS  Google Scholar 

  • Sato N-R, Hagio M, Wada H and Tsuzuki M (2000) Requirement of phosphatidylglycerol for photosynthetic function in thylakoid membranes. Proc Natl Acad Sci USA 97: 10655–10660

    Article  PubMed  CAS  Google Scholar 

  • Sato N-R, Tsuzuki M and Kawaguchi A (2003a) Glyceroli-pid synthesis in Chlorella kessleri 11h. I. Existence of a eukaryotic pathway. Biochim Biophys Acta 1633: 27–34

    Article  CAS  Google Scholar 

  • Sato N-R, Sugimoto K, Meguro A and Tsuzuki M (2003b) Identification of a gene for UDP-sulfoquinovose synthase of a green alga, Chlamydomonas reinhardtii, and its phy-logeny. DNA Res 10: 229–237

    Article  CAS  Google Scholar 

  • Sato S, Shimoda Y, Muraki A, Kohara M, Nakamura Y and Tabata S (2007) A large-scale protein-protein interaction analysis in Synechocystis sp. PCC 6803. DNA Res 14: 207–216

    Article  PubMed  CAS  Google Scholar 

  • Sayanova O, Smith MA, Lapinskas P, Stobart AK, Dobson G, Christie WW, Shewry PR and Napier JA (1997) Expression of a borage desaturase cDNA containing an N-terminal cytochrome b 5 domain results in the accumulation of high levels of Δ6-desaturated fatty acids in transgenic tobacco. Proc Natl Acad Sci USA 94: 4211–4216

    Article  PubMed  CAS  Google Scholar 

  • Schmidt H and Heinz E (1990a) Desaturation of oleoyl groups in envelope membranes from spinach chloroplasts. Proc Natl Acad Sci USA 87: 9477–9480

    Article  CAS  Google Scholar 

  • Schmidt H and Heinz E (1990b) Involvement of ferredoxin in desaturation of lipid-bound oleate in chloroplasts. Plant Physiol 94: 214–220

    Article  CAS  Google Scholar 

  • Selstam E and Campbell D (1996) Membrane lipid composition of the unusual cyanobacterium Gloeobacter violaceus sp. PCC 7421, which lacks sulfoquinovosyl diacylglyc-erol. Arch Microbiol 166: 132–135

    Article  CAS  Google Scholar 

  • Shimojima M, Ohta H, Iwamatsu A, Masuda T, Shioi Y and Takamiya K (1997) Cloning of the gene for monogalac-tosyldiacylglycerol synthase and its evolutionary origin. Proc Natl Acad Sci USA 94: 333–337

    Article  PubMed  CAS  Google Scholar 

  • Shimojima M, Hoffmann-Benning S, Garavito RM and Ben-ning C (2005) Ferredoxin-dependent glutamate synthase moonlights in plant sulfolipid biosynthesis by forming a complex with SQD1. Arch Biochem Biophys 436: 206–214

    Article  PubMed  CAS  Google Scholar 

  • Sinensky M (1974) Homeoviscous adaptation – a homeo-static process that regulates the viscosity of membrane lipids in Escherichia coli. Proc Natl Acad Sci USA 71: 522–525

    Article  PubMed  CAS  Google Scholar 

  • Singer SJ and Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175: 720–731

    Article  PubMed  CAS  Google Scholar 

  • Sperling P, Ternes P, Zank TK and Heinz E (2003) The evolution of desaturases. Prostaglandins Leukot Essent Fatty Acids 68: 73–95

    Article  PubMed  CAS  Google Scholar 

  • Stapleton SR and Jaworski JG (1984a) Characterization of fatty acid biosynthesis in the cyanobacterium Anabaena variabilis. Biochim Biophys Acta 794: 249–255

    Article  CAS  Google Scholar 

  • Stapleton SR and Jaworski JG (1984b) Characterization and purification of malonyl-coenzyme A: [acyl-carrier-protein] transacylases from spinach and Anabaena variabilis. Biochim Biophys Acta 794: 240–248

    Article  CAS  Google Scholar 

  • Suzuki I, Los DA, Kanesaki Y, Mikami K and Murata N (2000) The pathway for perception and transduction of low-temperature signals in Synechocystis. EMBO J 19: 1327–1334

    Article  PubMed  CAS  Google Scholar 

  • Suzuki I, Kanesaki Y, Mikami K, Kanehisa M and Murata N (2001) Cold-regulated genes under control of the cold sen sor Hik33 in Synechocystis. Mol Microbiol 40: 235–244

    Article  PubMed  CAS  Google Scholar 

  • Suzuki S, Ferjani A, Suzuki I and Murata N (2004) The SphS-SphR two component system is the exclusive sensor for the induction of gene expression in response to phosphate limitation in Synechocystis. J Biol Chem 279: 13234–13240

    Article  PubMed  CAS  Google Scholar 

  • Van Mooy BAS, Rocap G, Fredricks HF, Evans CT and Devol AH (2006) Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments. Proc Natl Acad Sci USA 103: 8607–8612

    Article  PubMed  CAS  Google Scholar 

  • Wada H and Murata N (1990) Temperature-induced changes in the fatty acid composition of the cyanobacterium, Syn-echocystis PCC 6803. Plant Physiol 92: 1062–1069

    Article  PubMed  CAS  Google Scholar 

  • Wada H and Murata N (1998) Membrane lipids in cyanobac-teria. In: Siegenthaler P-A and Murata N (eds) Lipids in Photosynthesis: Structure, Function and Genetics. Kluwer, Dordrecht, pp. 65–81

    Google Scholar 

  • Wada H, Gombos Z and Murata N (1990) Enhancement of chilling tolerance of a cyanobacterium by genetic manipulation of fatty acid desaturation. Nature 347: 200–203

    Article  PubMed  CAS  Google Scholar 

  • Wada H, Schmidt H, Heinz E and Murata N (1993a) In vitro ferredoxin-dependent desaturation of fatty acids in cyano-bacterial thylakoid membranes. J Bacteriol 175: 544–547

    CAS  Google Scholar 

  • Wada H, Avelange-Macherel MH and Murata N (1993b) The desA gene of the cyanobacterium Synechocystis sp. strain PCC 6803 is the structural gene for Δ12 desaturase. J Bacteriol 175: 6056–6058

    CAS  Google Scholar 

  • Wakil SJ, Stoops JK and Joshi VC (1983) Fatty acid synthesis and its regulation. Annu Rev Biochem 52: 537–579

    Article  PubMed  CAS  Google Scholar 

  • Weier D, Müller C, Gaspers C and Frentzen M (2005) Characterization of acyltransferases from Synechocystis sp. PCC 6803. Biochem Biophys Res Commun 334: 1127–1134

    Article  PubMed  CAS  Google Scholar 

  • Weissenmayer B, Geiger O and Benning C (2000) Disruption of a gene essential for sulfoquinovosyldiacylglycerol biosynthesis in Sinorhizobium meliloti has no detectable effect on root nodule symbiosis. Mol Plant Microbe Interact 13: 666–672

    Article  PubMed  CAS  Google Scholar 

  • Wu F, Yang Z and Kuang T (2006) Impaired photosynthesis in phosphatidylglycerol-deficient mutant of cyanobac-terium Anabaena sp. PCC 7120 with a disrupted gene encoding a putative phosphatidylglycerophosphatase. Plant Physiol 141: 1274–1283

    Article  PubMed  CAS  Google Scholar 

  • Xu C, Härtel H, Wada H, Hagio M, Yu B, Eakin C and Ben-ning C (2002) The pgp1 mutant locus of Arabidopsis encodes a phosphatidylglycerolphosphate synthase with impaired activity. Plant Physiol 129: 594–604

    Article  PubMed  CAS  Google Scholar 

  • Yu B and Benning C (2003) Anionic lipids are required for chloroplast structure and function in Arabidopsis. Plant J 36: 762–770

    Article  PubMed  CAS  Google Scholar 

  • Yu B, Xu C and Benning C (2002) Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc Natl Acad Sci USA 99: 5732–5737

    Article  PubMed  CAS  Google Scholar 

  • Yu B, Wakao S, Fan J and Benning C (2004) Loss of plastidic lysophosphatidic acid acyltransferase causes embryo-lethality in Arabidopsis. Plant Cell Physiol 45: 503–510

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported in part by Grants-in-Aid from the Promotion and Mutual Aid Corporation for Private Schools of Japan and by a Grant-in-Aid for Scientific Research (no. 20570031) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Norihiro Sato .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Sato, N., Wada, H. (2009). Lipid Biosynthesis and its Regulation in Cyanobacteria. In: Wada, H., Murata, N. (eds) Lipids in Photosynthesis. Advances in Photosynthesis and Respiration, vol 30. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-2863-1_8

Download citation

Publish with us

Policies and ethics