slr2103, a homolog of type-2 diacylglycerol acyltransferase genes, for plastoquinone-related neutral lipid synthesis and NaCl-stress acclimatization in a cyanobacterium, Synechocystis sp. PCC 6803

Abstract

A cyanobacterium, Synechocystis sp. PCC 6803, contains a lipid with triacylglycerol-like TLC mobility but its identity and physiological roles remain unknown. Here, on ESI-positive LC-MS2 analysis, it is shown that the triacylglycerol-like lipid (lipid X) is related to plastoquinone and can be grouped into two subclasses, Xa and Xb, the latter of which is esterified by 16:0 and 18:0. This study further shows that a Synechocystis homolog of type-2 diacylglycerol acyltransferase genes, slr2103, is essential for lipid X synthesis: lipid X disappears in a Synechocystis slr2103-disruptant whereas it appears in an slr2103-overexpressing transformant (OE) of Synechococcus elongatus PCC 7942 that intrinsically lacks lipid X. The slr2103 disruption causes Synechocystis cells to accumulate plastoquinone-C at an abnormally high level whereas slr2103 overexpression in Synechococcus causes the cells to almost completely lose it. It is thus deduced that slr2103 encodes a novel acyltransferase that esterifies 16:0 or 18:0 with plastoquinone-C for the synthesis of lipid Xb. Characterization of the slr2103-disruptant in Synechocystis shows that slr2103 contributes to sedimented-cell growth in a static culture, and to bloom-like structure formation and its expansion by promoting cell aggregation and floatation upon imposition of saline stress (0.3-0.6 M NaCl). These observations provide a basis for elucidation of the molecular mechanism of a novel cyanobacterial strategy to acclimatize to saline stress, and one for development of a system of seawater-utilization and economical harvesting of cyanobacterial cells with high-value added compounds, or blooming control of toxic cyanobacteria.

Plastoquinone Lipids: Their Synthesis via a Bifunctional Gene and Physiological Function in a Euryhaline Cyanobacterium, Synechococcus sp. PCC 7002

“…However, no conclusion has been drawn concerning the physiological roles of PQ-B in seed plants, PQ-B deficient mutants of which are unavailable, with no genes identified for PQ-B synthesis. Meanwhile, PQ lipids or slr2103 have been shown to be crucial in Synechococystis 6803 for the growth of cells as a sediment in a static culture [ 3 ]. It is of particular note that PQ lipids or slr2103 have been shown to facilitate the formation of a pellicle biofilm in Synechococystis 6803 cells under NaCl-stress conditions, thereby, allowing them to rapidly grow, owing to the high availability of CO 2 and light energy for photosynthesis [ 3 ].…”

“…Meanwhile, PQ lipids or slr2103 have been shown to be crucial in Synechococystis 6803 for the growth of cells as a sediment in a static culture [ 3 ]. It is of particular note that PQ lipids or slr2103 have been shown to facilitate the formation of a pellicle biofilm in Synechococystis 6803 cells under NaCl-stress conditions, thereby, allowing them to rapidly grow, owing to the high availability of CO 2 and light energy for photosynthesis [ 3 ]. In this context, it is of interest that homologs of slr2103 are present in numerous cyanobacteria collected from a wide variety of habitats that would least encounter fluctuations in saline stress, however, with the exclusion of oceanic Synechococcus and Prochlorococcus strains [ 3 ].…”

“…It is of particular note that PQ lipids or slr2103 have been shown to facilitate the formation of a pellicle biofilm in Synechococystis 6803 cells under NaCl-stress conditions, thereby, allowing them to rapidly grow, owing to the high availability of CO 2 and light energy for photosynthesis [ 3 ]. In this context, it is of interest that homologs of slr2103 are present in numerous cyanobacteria collected from a wide variety of habitats that would least encounter fluctuations in saline stress, however, with the exclusion of oceanic Synechococcus and Prochlorococcus strains [ 3 ]. In addition, PQ lipid or slr2103 -dependent formation of a pellicle biofilm has increased the potential to industrially utilize the gene for concentration of high-added-value biomass in photosynthetic microorganisms [ 3 ].…”

“…In this context, it is of interest that homologs of slr2103 are present in numerous cyanobacteria collected from a wide variety of habitats that would least encounter fluctuations in saline stress, however, with the exclusion of oceanic Synechococcus and Prochlorococcus strains [ 3 ]. In addition, PQ lipid or slr2103 -dependent formation of a pellicle biofilm has increased the potential to industrially utilize the gene for concentration of high-added-value biomass in photosynthetic microorganisms [ 3 ]. Moreover, notably, slr2103 homologs are present in cyanobacterial species that naturally bloom such as Microcystis [ 3 ].…”

“…In addition, PQ lipid or slr2103 -dependent formation of a pellicle biofilm has increased the potential to industrially utilize the gene for concentration of high-added-value biomass in photosynthetic microorganisms [ 3 ]. Moreover, notably, slr2103 homologs are present in cyanobacterial species that naturally bloom such as Microcystis [ 3 ]. Therefore, elucidation of the molecular function of PQ lipids in the pellicle biofilm formation in Synechocystis would lead to a better understanding of the molecular mechanism of cyanobacterial natural blooms and accordingly would provide clues to control it [ 3 ].…”