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Research Article

Triacylglycerol and phytyl ester synthesis in Synechocystis sp. PCC6803

Mohammed Aizouq, Helga Peisker, Katharina Gutbrod, Michael Melzer, Georg Hölzl, and View ORCID ProfilePeter Dörmann
  1. aInstitute of Molecular Physiology and Biotechnology of Plants, University of Bonn, 53115 Bonn, Germany;
  2. bDepartment of Physiology and Cell Biology, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Seeland, OT Gatersleben, Germany

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PNAS March 17, 2020 117 (11) 6216-6222; first published March 2, 2020; https://doi.org/10.1073/pnas.1915930117
Mohammed Aizouq
aInstitute of Molecular Physiology and Biotechnology of Plants, University of Bonn, 53115 Bonn, Germany;
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Helga Peisker
aInstitute of Molecular Physiology and Biotechnology of Plants, University of Bonn, 53115 Bonn, Germany;
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Katharina Gutbrod
aInstitute of Molecular Physiology and Biotechnology of Plants, University of Bonn, 53115 Bonn, Germany;
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Michael Melzer
bDepartment of Physiology and Cell Biology, Leibniz Institute of Plant Genetics and Crop Plant Research, 06466 Seeland, OT Gatersleben, Germany
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Georg Hölzl
aInstitute of Molecular Physiology and Biotechnology of Plants, University of Bonn, 53115 Bonn, Germany;
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Peter Dörmann
aInstitute of Molecular Physiology and Biotechnology of Plants, University of Bonn, 53115 Bonn, Germany;
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  • ORCID record for Peter Dörmann
  • For correspondence: doermann@uni-bonn.de
  1. Edited by Krishna K. Niyogi, University of California, Berkeley, CA, and approved February 3, 2020 (received for review September 16, 2019)

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Significance

Cyanobacteria harbor a photosynthetic apparatus related to plant chloroplasts. The lipid compositions of the thylakoids that harbor the photosynthetic complexes in cyanobacteria and chloroplasts are highly similar. Chloroplasts contain triacylglycerol (storage oil) and wax esters; the latter are composed of phytol derived from chlorophyll and fatty acids (phytyl esters). However, the existence of these lipids in cyanobacteria in general remained unclear. Here we show that the cyanobacterium Synechocystis contains triacylglycerol and phytyl esters. A mutant, Δslr2103, was generated, which lacked these two lipids but showed no obvious growth defect. The slr2103 gene encodes a diacylglycerol acyltransferase different from known enzymes of triacylglycerol synthesis in bacteria. This pathway can be employed to produce oil for biotechnological applications in cyanobacteria.

Abstract

Cyanobacteria are unicellular prokaryotic algae that perform oxygenic photosynthesis, similar to plants. The cells harbor thylakoid membranes composed of lipids related to those of chloroplasts in plants to accommodate the complexes of photosynthesis. The occurrence of storage lipids, including triacylglycerol or wax esters, which are found in plants, animals, and some bacteria, nevertheless remained unclear in cyanobacteria. We show here that the cyanobacterium Synechocystis sp. PCC6803 accumulates both triacylglycerol and wax esters (fatty acid phytyl esters). Phytyl esters accumulate in higher levels under abiotic stress conditions. The analysis of an insertional mutant revealed that the acyltransferase slr2103, with sequence similarity to plant esterase/lipase/thioesterase (ELT) proteins, is essential for triacylglycerol and phytyl ester synthesis in Synechocystis. The recombinant slr2103 enzyme showed acyltransferase activity with phytol and diacylglycerol, thus producing phytyl esters and triacylglycerol. Acyl-CoA thioesters were the preferred acyl donors, while acyl-ACP (acyl carrier protein), free fatty acids, or galactolipid-bound fatty acids were poor substrates. The slr2103 protein sequence is unrelated to acyltransferases from bacteria (AtfA) or plants (DGAT1, DGAT2, PDAT), and therefore establishes an independent group of bacterial acyltransferases involved in triacylglycerol and wax ester synthesis. The identification of the gene slr2103 responsible for triacylglycerol synthesis in cyanobacteria opens the possibility of using prokaryotic photosynthetic cells in biotechnological applications.

  • cyanobacteria
  • triacylglycerol
  • wax
  • acyltransferase

Footnotes

  • ↵1To whom correspondence may be addressed. Email: doermann{at}uni-bonn.de.
  • Author contributions: G.H. and P.D. designed research; M.A. and M.M. performed research; M.A., H.P., K.G., and M.M. contributed new reagents/analytic tools; M.A., H.P., K.G., G.H., and P.D. analyzed data; and M.A. and P.D. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1915930117/-/DCSupplemental.

Published under the PNAS license.

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Triacylglycerol and phytyl ester synthesis in Synechocystis sp. PCC6803
Mohammed Aizouq, Helga Peisker, Katharina Gutbrod, Michael Melzer, Georg Hölzl, Peter Dörmann
Proceedings of the National Academy of Sciences Mar 2020, 117 (11) 6216-6222; DOI: 10.1073/pnas.1915930117

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Triacylglycerol and phytyl ester synthesis in Synechocystis sp. PCC6803
Mohammed Aizouq, Helga Peisker, Katharina Gutbrod, Michael Melzer, Georg Hölzl, Peter Dörmann
Proceedings of the National Academy of Sciences Mar 2020, 117 (11) 6216-6222; DOI: 10.1073/pnas.1915930117
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Proceedings of the National Academy of Sciences: 117 (11)
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