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

• Published in: Plant physiology (Bethesda) 2016-11, Vol.172 (3), p.1928-1940
• Main Authors: Lea-Smith, David J., Ortiz-Suarez, Maite L., Lenn, Tchern, Nürnberg, Dennis J., Baers, Laura L., Davey, Matthew P., Parolini, Lucia, Huber, Roland G., Cotton, Charles A.R., Mastroianni, Giulia, Bombelli, Paolo, Ungerer, Petra, Stevens, Tim J., Smith, Alison G., Bond, Peter J., Mullineaux, Conrad W., Howe, Christopher J.
• Format: Article
• Language: English
• Subjects: Biosynthetic Pathways - drug effects; Cell Division - drug effects; Cell Proliferation - drug effects; Hydrocarbons - pharmacology; Intracellular Membranes - drug effects; Intracellular Membranes - metabolism; Lipid Bilayers - metabolism; MEMBRANES, TRANSPORT, AND BIOENERGETICS; Mutation - genetics; Photosynthesis - drug effects; Synechocystis - cytology; Synechocystis - drug effects; Synechocystis - growth & development; Synechocystis - metabolism; Thylakoids - drug effects; Thylakoids - metabolism
• ISSN: 0032-0889; 1532-2548; 1532-2548
• DOI: 10.1104/pp.16.01205

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 andmembrane-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.