Skip to main content

Composition and occurrence of lipid droplets in the cyanobacterium Nostoc punctiforme

Archives of Microbiology volume 196, pages 881–890 (2014)Cite this article

Abstract

Inclusions of neutral lipids termed lipid droplets (LDs) located throughout the cell were identified in the cyanobacterium Nostoc punctiforme by staining with lipophylic fluorescent dyes. LDs increased in number upon entry into stationary phase and addition of exogenous fructose indicating a role for carbon storage, whereas high-light stress did not increase LD numbers. LD accumulation increased when nitrate was used as the nitrogen source during exponential growth as compared to added ammonia or nitrogen-fixing conditions. Analysis of isolated LDs revealed enrichment of triacylglycerol (TAG), α-tocopherol, and C17 alkanes. LD TAG from exponential phase growth contained mainly saturated C16 and C18 fatty acids, whereas stationary phase LD TAG had additional unsaturated fatty acids characteristic of whole cells. This is the first characterization of cyanobacterial LD composition and conditions leading to their production. Based upon their abnormally large size and atypical location, these structures represent a novel sub-organelle in cyanobacteria.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Allen M, Arnon DI (1955) Studies on nitrogen-fixing blue-green algae. I. Growth and nitrogen fixation by Anabaena cylindrica Lemm. Plant Physiol 30:366–372

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Austin JR, Frost E, Vidi P-A, Kessler F, Staehelina LA (2006) Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes. Plant Cell 18:1693–1703

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Besagni C, Kessler F (2013) A mechanism implicating plastoglobules in thylakoid disassembly during senescence and nitrogen starvation. Planta 237:463–470

    CAS  PubMed  Article  Google Scholar 

  • Bligh E, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    CAS  PubMed  Article  Google Scholar 

  • Boudière L et al (2014) Glycerolipids in photosynthesis: composition, synthesis and trafficking. Biochim et Biophys Acta (BBA) Bioenerg 1837:470–480

    Article  Google Scholar 

  • Bréhélin C, Kessler F (2008) The plastoglobule: a bag full of lipid biochemistry tricks. Photochem Photobiol 84:1388–1394

    PubMed  Article  Google Scholar 

  • Chapman KD, Dyer JD, Mullen RT (2012) Biogenesis and functions of lipid droplets in plants. J Lipid Res 53:215–226

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Cooper MS, Hardin WR, Petersen TW, Cattolico RA (2010) Visualizing “green oil” in live algal cells. J Biosci Bioeng 109:198–201

    CAS  PubMed  Article  Google Scholar 

  • Cunningham FX, Tice AB, Pham C, Gantt E (2010) Inactivation of genes encoding plastoglobulin-like proteins in Synechocystis sp. PCC 6803 leads to a light-sensitive phenotype. J Bacteriol 192:1700–1709

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Deruere J, Romer S, d’Harlingue A, Backhaus R, Kuntz M, Camara B (1994) Fibril assembly and carotenoid overaccumulation in chromoplasts: a model for supramolecular lipoprotein structures. Plant Cell 6:119–133

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Ding Y et al (2012) Identification of the major functional proteins of prokaryotic lipid droplets. J Lipid Res 53:399–411

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Edwards MR, Berns DS, Ghiorse WC, Holt SC (1968) Ultrastructure of the thermophilic blue-green alga, Synechococcus lividus Copeland. J Phycol 4:283–298

    Article  Google Scholar 

  • Fan J, Yan C, Andre C, Shanklin J, Schwender J, Xu C (2012) Oil accumulation is controlled by carbon precursor supply for fatty acid synthesis in Chlamydomonas reinhardtii. Plant Cell Physiol 53:1380–1390

    CAS  PubMed  Article  Google Scholar 

  • Farese RVJ, Walther TC (2009) Lipid droplets finally get a little R-E-S-P-E-C-T. Cell 139:855–860

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Goodson C, Wang ZT, Goodenough U (2011) Structural correlates of cytoplasmic and chloroplast lipid body synthesis in Chlamydomonas reinhardtii and stimulation of lipid body production with acetate boost. Eukaryot Cell 10:1592–1606

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Havaux M, Eymery F, Porfirova S, Pascal Rey P, Peter Dörmann P (2005) Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 17:3451–3469

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Hu Q et al (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54:621–639

    CAS  PubMed  Article  Google Scholar 

  • Hutchins PM, Barkley RM, Murphy RC (2008) Separation of cellular nonpolar neutral lipids by normal-phase chromatography and analysis by electrospray ionization mass spectrometry. J Lipid Res 49:804–813

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Jacquier N, Mishra S, Choudhary V, Schneiter R (2013) Expression of oleosin and perilipins in yeast promote formation of lipid droplets from the endoplasmatic reticulum. J Cell Sci 126:5198–5209

    CAS  PubMed  Article  Google Scholar 

  • Kessler F, Vidi P-A (2007) Plastoglobule lipid bodies: their functions in chloroplasts and their potential for applications. Adv Biochem Eng/Biotechnol 107:153–172

    CAS  Article  Google Scholar 

  • Khandelia H, Duelund L, Pakkanen KI, Ipsen JH (2010) Triglyceride blisters in lipid bilayers: implications for lipid droplet biogenesis and the mobile lipid signal in cancer cell membranes. PLoS ONE 5:e12811

    PubMed Central  PubMed  Article  Google Scholar 

  • Kuroiwa T et al (2012) Lipid droplets of bacteria, algae and fungi and a relationship between their contents and genome sizes as revealed by BODIPY and DAPI staining. Cytologia 77:289–299

    Article  Google Scholar 

  • Lichtenthaler HK (2007) Biosynthesis, accumulation and emission of carotenoids, α-tocopherol, plastoquinone, and isoprene in leaves under high photosynthetic irradiance. Photosynth Res 92:163–179

    CAS  PubMed  Article  Google Scholar 

  • Maeda K et al (2005) Adipocyte/macrophage fatty acid binding proteins control integrated metabolic responses in obesity and diabetes. Cell Metab 1:107–119

    CAS  PubMed  Article  Google Scholar 

  • Meeks JC, Campbell EL, Summers ML, Wong FC (2002) Cellular differentiation in the cyanobacterium Nostoc punctiforme. Arch Microbiol 178:395–403

    CAS  PubMed  Article  Google Scholar 

  • Miao XL, Wu QY (2006) Biodiesel production from heterotrophic microalgal oil. Bioresour Tech 97:841–846

    CAS  Article  Google Scholar 

  • Moellering ER, Miller R, Benning C (2009) Molecular genetics of lipid metabolism in the model green alga Chlamydomonas reinhardtii. In: Wada H, Murata M (eds) Lipids in photosynthesis: essential and regulatory functions. Springer, Dordrecht, pp 139–150

    Chapter  Google Scholar 

  • Murphy DJ (2012) The dynamic roles of intracellular lipid droplets: from archaea to mammals. Protoplasma 249:541–585

    CAS  PubMed  Article  Google Scholar 

  • Murphy DJ, Vance J (1999) Mechanisms of lipid-body formation. TIBS 24:109–115

    CAS  PubMed  Google Scholar 

  • Nierswicki-Bauer SA, Balkwill DL, Stevens SE Jr (1983) Three-dimensional ultrastructure of a unicellular cyanobacterium. J Cell Biol 97:713–722

    Article  Google Scholar 

  • Pankratz HS, Bowen CC (1963) Cytology of blue-green algae. I. The cells of Symploca muscorum. Am J Bot 50:387–399

    Article  Google Scholar 

  • Piller LE, Abraham M, Dormann P, Kessler F, Besagni C (2012) Plastid lipid droplets at the crossroads of prenylquinone metabolism. J Exp Bot 63:1609–1618

    Article  Google Scholar 

  • Rey P et al (2000) Over-expression of a pepper plastid lipid-associated protein in tobacco leads to changes in plastid ultrastructure and plant development upon stress. Plant J 21:483–494

    CAS  PubMed  Article  Google Scholar 

  • Schirmer A, Rude MA, Li X, Popova E, del Cardayre SB (2010) Microbial biosynthesis of alkanes. Science 329:559–562

    CAS  PubMed  Article  Google Scholar 

  • Selvan BK, Revathi M, Piriya PS, Vasan PT, Prabhu DIG, Vennison SJ (2013) Biodiesel production from marine cyanobacteria culture in plate and tubular photobioreactors. Ind J Exp Biol 51:262–268

    CAS  Google Scholar 

  • Sheng J, Vannela R, Rittmann BE (2011) Evaluation of methods to extract and quantify lipids from Synechocystis PCC 6803. Bioresour Tech 102:1697–1703

    CAS  Article  Google Scholar 

  • van de Meene AML, Hohmann-Marriott MF, Vermaas WFJ, Roberson RW (2006) The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803. Arch Micrbiol 184:259–270

    CAS  Article  Google Scholar 

  • Vidi P-A et al (2006) Tocopherol cyclase (VTE1) localization and vitamin E accumulation in chloroplast plastoglobule lipoprotein particles. J Biol Chem 281:11225–11234

    CAS  PubMed  Article  Google Scholar 

  • Wang ZT, Ullrich N, Joo S, Waffenschidt S, Goodenough U (2009) Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii. Eukaryot Cell 8:1856–1868

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Wolk CP (1973) Physiology and cytological chemistry of blue-green algae. Bacteriol Rev 37:32–101

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wolk CP, Ernst A, Elhai J (1994) Heterocyst metabolism and development. In: Bryant DA (ed) The molecular biology of cyanobacteria. Kluwer, Dordrecht, pp 769–823

    Chapter  Google Scholar 

  • Yang L et al (2012) The proteomics of lipid droplets: structure, dynamics, and functions of the organelle conserved from bacteria to humans. J Lipid Res 53:1245–1253

    CAS  PubMed Central  PubMed  Article  Google Scholar 

Download references

Acknowledgments

This work was supported by National Institutes of Health Grant SC1 GM093998-01, National Science Foundation Grant MCB-1413583, and funding from California State University Program for Education and Research in Biotechnology (CSUPERB) to MLS.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Affiliations

  1. Department of Biology, California State University Northridge, 18111 Nordhoff St., Northridge, CA, 91330-8303, USA

    Anantha Peramuna & Michael L. Summers

Authors
  1. Anantha Peramuna
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael L. Summers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael L. Summers.

Additional information

Communicated by Erko Stackebrandt.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Peramuna, A., Summers, M.L. Composition and occurrence of lipid droplets in the cyanobacterium Nostoc punctiforme . Arch Microbiol 196, 881–890 (2014). https://doi.org/10.1007/s00203-014-1027-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-014-1027-6

Keywords

  • Neutral lipid droplet
  • Cyanobacteria
  • Triacylglycerol
  • α-Tocopherol
  • Alkane production