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

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.

Terminal Olefin Profiles and Phylogenetic Analyses of Olefin Synthases of Diverse Cyanobacterial Species

“…The physiological roles of cyanobacterial hydrocarbons, which are involved in introducing flexibility into membranes and are required for optimal cell division, size, and growth, have been previously reported (7). Though strains harboring the Ols pathway have been proposed to account for a small proportion (approximately 10%) of the cyanobacterial population (4, 5), hydrocarbon production in such strains is recog-…”

“…The subcellular location of hydrocarbons is within the lipid bilayers of thylakoid and cytoplasmic membranes, and the biological function of hydrocarbons is thought to be associated with the membrane flexibility required for optimal cell division, size, and growth (7). Free fatty acids in cyanobacteria are thought to be released from complex membrane lipids (8).…”

The Development of Biophotovoltaic Systems for Power Generation and Biological Analysis

“…[10,[14][15][16][17][18][19][20] It is a unicellular coccoid organism, with diameter around 1.6 μm, although this is altered in some mutant strains. [21] Some cyanobacteria, such as Synechococcus elongatus PCC7942, [22,23] which is also commonly used, have more elongated cells. Others, such as Nostoc, [24,25] routinely form filaments.…”

Proteome Mapping of a Cyanobacterium Reveals Distinct Compartment Organization and Cell-Dispersed Metabolism

“…In addition, isolating membranes via two-phase aqueous polymer partitioning results in considerable losses of cellular material and undersampling of the proteome. Furthermore, both the PM and TM may be heterogeneous (Srivastava et al, 2006;Agarwal et al, 2010;Pisareva et al, 2011) and previous work has suggested that only a hydrocarbon-rich fraction of the TM, and not the whole membrane, is purified via two-phase partitioning (Lea-Smith et al, 2016b). For example, a highly curved 'convergence membrane' substructure in the TM was recently observed, which was in close contact with the PM, and may play a role in biogenesis of thylakoid proteins (Rast et al, 2019).…”

“…For example, these methods have been shown to give 'purified' PM fractions that actually contain detectable amounts of TM (e.g. Zhang et al, 2015;Lea-Smith et al, 2016b). In addition, isolating membranes via two-phase aqueous polymer partitioning results in considerable losses of cellular material and undersampling of the proteome.…”