Multifunctional acyltransferases involved in the synthesis of triacylglycerol, fatty acid phytyl esters and plastoquinol esters in cyanobacteria.

Main conclusion: The multifunctional acyltransferases (MFAT) from Synechocystis sp. PCC 6803 and Synechococcus sp. PCC 7002 synthesize triacylglycerol, fatty acid phytyl esters, acylated plastoquinol-9 and acylated plastoquinone C, while Gloeobacter violaceus PCC 7421 synthesizes acylated plastoquinol-9 in an MFAT-independent pathway. Cyanobacteria contain large amounts of polar lipids in their thylakoid membranes, but the contents of nonpolar lipids are low. We previously identified triacylglycerol (TAG) and fatty acid phytyl esters (FAPE) in Synechocystis sp. PCC 6803, and described a gene (slr2103) involved in TAG and FAPE synthesis. Other studies showed that Synechocystis sp. PCC 6803 and Synechococcus sp. PCC 7002 synthesizes acylated forms of plastoquinol-9 (acyl-PQH) and of plastoquinone C (acyl-PQC), which carries the fatty acid on a hydroxyl group on the isoprenoid chain, but TAG and FAPE were not detected. We confirm here that Synechocystis sp. PCC 6803 and Synechococcus sp. PCC 7002 contain TAG, FAPE, acyl-PQH and acyl-PQC. Expression of slr2103 and the related gene A0918 from Synechococcus sp. PCC 7002 in Escherichia coli, and analysis of the respective cyanobacterial mutants revealed that the two proteins acylate diacylglycerol, phytol, and the plastoquinol-9 analog decylplastoquinol. Therefore, slr2103 and A0918 encode multifunctional acyltransferases (MFAT) with broad substrate specificities. Gloeobacter violaceus PCC 7421, a primitive cyanobacterium that lacks an MFAT-like gene, accumulates acyl-PQH, indicating that this strain harbors an MFAT-independent acyltransferase capable of acylating plastoquinol-9. These results demonstrate that cyanobacteria synthesize different nonpolar lipids including TAG, FAPE and acylated forms of plastoquinol, employing MFAT-dependent and MFAT-independent pathways.