Abstract
The ability to produce medium chain length aliphatic hydrocarbons is strictly conserved in all photosynthetic cyanobacteria, but the molecular function and biological significance of these compounds still remain poorly understood. This study gives a detailed view to the changes in intracellular hydrocarbon chain saturation in response to different growth temperatures and osmotic stress, and the associated physiological effects in the model cyanobacterium Synechocystis sp. PCC 6803. We show that the ratio between the representative hydrocarbons, saturated heptadecane and desaturated heptadecene, is reduced upon transition from 38°C toward 15°C, while the total content is not much altered. In parallel, it appears that in the hydrocarbon-deficient ∆ado (aldehyde deformylating oxygenase) mutant, phenotypic and metabolic changes become more evident under suboptimal temperatures. These include hindered growth, accumulation of polyhydroxybutyrate, altered pigment profile, restricted phycobilisome movement, and ultimately reduced CO2 uptake and oxygen evolution in the ∆ado strain as compared to Synechocystis wild type. The hydrocarbons are present in relatively low amounts and expected to interact with other nonpolar cellular components, including the hydrophobic part of the membrane lipids. We hypothesize that the function of the aliphatic chains is specifically associated with local fluidity effects of the thylakoid membrane, which may be required for the optimal movement of the integral components of the photosynthetic machinery. The findings support earlier studies and expand our understanding of the biological role of aliphatic hydrocarbons in acclimation to low temperature in cyanobacteria and link the proposed role in the thylakoid membrane to changes in photosynthetic performance, central carbon metabolism, and cell growth, which need to be effectively fine-tuned under alternating conditions in nature.
Highlights
Unlike prokaryotes in general, all known photosynthetic cyanobacteria harbor the capacity to produce aliphatic hydrocarbons in their native metabolism (Coates et al, 2014; Lea-Smith et al, 2015)
Despite the explicit conservation throughout evolution, hydrocarbons have not been found to be essential for cyanobacteria under any tested laboratory conditions, and the biosynthetic pathways can be disrupted without compromising the viability of the cells: Inactivation of hydrocarbon biosynthesis has been reported to result in reduced growth (Berla et al, 2015; Lea-Smith et al, 2016) and defected cell division under photoautotrophic conditions (Lea-Smith et al, 2016) in the cyanobacterial model strains Synechocystis sp
In order to select specific native alkanes and alkenes for the target profiling, Synechocystis cell extracts were subjected to GC–MS analysis against commercial standards for the ions m/z 55, m/z 57, and m/z = 83 to identify C15 and C17 hydrocarbon species typically found in cyanobacteria (Tan et al, 2011; Coates et al, 2014; Supplementary Figure S1)
Summary
All known photosynthetic cyanobacteria harbor the capacity to produce aliphatic hydrocarbons in their native metabolism (Coates et al, 2014; Lea-Smith et al, 2015). Hydrocarbons have been found in the cyanobacterial lipid fractions and as part of the thylakoid membranes (Lea-Smith et al, 2016), which harbor the photosynthetic apparatus and associated protein complexes. In this context, hydrocarbons have been reported to serve as structural components that stack together and enhance the thylakoid membrane curvature (Lea-Smith et al, 2016), which again may have an influence on the topology, movement, and dynamic interplay of the embedded integral proteins. The observed effects include enhanced cyclic electron flow as recorded under reduced temperatures, possibly in response changes in the intracellular ATP:NADPH ratio (Berla et al, 2015), and alterations in the photosystem (PS) II/I ratio, phycobilisome coupling, and oxygen uptake, without any significant changes on the net O2 evolution (Lea-Smith et al, 2016)
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