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Plant Physiol. 2016 Nov;172(3):1928-1940. Epub 2016 Oct 5.

Hydrocarbons Are Essential for Optimal Cell Size, Division, and Growth of Cyanobacteria.

Lea-Smith DJ1,2,3,4,5,6,7,8, Ortiz-Suarez ML9,10,11,12,13,14,15,16, Lenn T9,10,11,12,13,14,15,16, Nürnberg DJ9,10,11,12,13,14,15,16, Baers LL9,10,11,12,13,14,15,16, Davey MP9,10,11,12,13,14,15,16, Parolini L9,10,11,12,13,14,15,16, Huber RG9,10,11,12,13,14,15,16, Cotton CA9,10,11,12,13,14,15,16, Mastroianni G9,10,11,12,13,14,15,16, Bombelli P9,10,11,12,13,14,15,16, Ungerer P9,10,11,12,13,14,15,16, Stevens TJ9,10,11,12,13,14,15,16, Smith AG9,10,11,12,13,14,15,16, Bond PJ9,10,11,12,13,14,15,16, Mullineaux CW9,10,11,12,13,14,15,16, Howe CJ9,10,11,12,13,14,15,16.

Author information

1
Department of Biochemistry, University of Cambridge, Cambridge CB2 1QW, United Kingdom (D.J.L.-S., L.L.B., C.A.R.C., P.B., C.J.H.); djl63@cam.ac.uk.
2
Centre for Molecular Science Informatics, Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, United Kingdom (M.L.O.-S., P.J.B.); djl63@cam.ac.uk.
3
School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, United Kingdom (T.L., D.J.N., G.M., P.U., C.W.M.); djl63@cam.ac.uk.
4
Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom (M.P.D., A.G.S.); djl63@cam.ac.uk.
5
Department of Physics, University of Cambridge, Cambridge CB3 0HE, United Kingdom (L.P.); djl63@cam.ac.uk.
6
Bioinformatics Institute, A*STAR, Singapore 138671 (R.G.H., P.J.B.); djl63@cam.ac.uk.
7
MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, United Kingdom (T.J.S.); and djl63@cam.ac.uk.
8
National University of Singapore, Department of Biological Sciences, Singapore 117543 (P.J.B.) djl63@cam.ac.uk.
9
Department of Biochemistry, University of Cambridge, Cambridge CB2 1QW, United Kingdom (D.J.L.-S., L.L.B., C.A.R.C., P.B., C.J.H.).
10
Centre for Molecular Science Informatics, Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, United Kingdom (M.L.O.-S., P.J.B.).
11
School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, United Kingdom (T.L., D.J.N., G.M., P.U., C.W.M.).
12
Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom (M.P.D., A.G.S.).
13
Department of Physics, University of Cambridge, Cambridge CB3 0HE, United Kingdom (L.P.).
14
Bioinformatics Institute, A*STAR, Singapore 138671 (R.G.H., P.J.B.).
15
MRC Laboratory of Molecular Biology, Cambridge CB2 0QH, United Kingdom (T.J.S.); and.
16
National University of Singapore, Department of Biological Sciences, Singapore 117543 (P.J.B.).

Abstract

Cyanobacteria are intricately organized, incorporating an array of internal thylakoid membranes, the site of photosynthesis, into cells no larger than other bacteria. They also synthesize C15-C19 alkanes and alkenes, which results in substantial production of hydrocarbons in the environment. All sequenced cyanobacteria encode hydrocarbon biosynthesis pathways, suggesting an important, undefined physiological role for these compounds. Here, we demonstrate that hydrocarbon-deficient mutants of Synechococcus sp. PCC 7002 and Synechocystis sp. PCC 6803 exhibit significant phenotypic differences from wild type, including enlarged cell size, reduced growth, and increased division defects. Photosynthetic rates were similar between strains, although a minor reduction in energy transfer between the soluble light harvesting phycobilisome complex and membrane-bound photosystems was observed. Hydrocarbons were shown to accumulate in thylakoid and cytoplasmic membranes. Modeling of membranes suggests these compounds aggregate in the center of the lipid bilayer, potentially promoting membrane flexibility and facilitating curvature. In vivo measurements confirmed that Synechococcus sp. PCC 7002 mutants lacking hydrocarbons exhibit reduced thylakoid membrane curvature compared to wild type. We propose that hydrocarbons may have a role in inducing the flexibility in membranes required for optimal cell division, size, and growth, and efficient association of soluble and membrane bound proteins. The recent identification of C15-C17 alkanes and alkenes in microalgal species suggests hydrocarbons may serve a similar function in a broad range of photosynthetic organisms.

PMID:
27707888
PMCID:
PMC5100757
DOI:
10.1104/pp.16.01205
[Indexed for MEDLINE]
Free PMC Article

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