Occurrence of sucrose metabolism in bloom-forming cyanobacteria

M.A. KOLMAN; G.L. SALERNO

Texel

Workshop; 9th European Workshop on Molecular Biology of Cyanobacteria; 2014

NIOZ and Federation of European Microbiological Societies

Studies in cyanobacteria and the availability of complete genome sequences have significantly increased our knowledge of the structure of proteins involved in sucrose (Suc) metabolism, their origin and further evolution. Studies in nitrogen-fixing filamentous strains and in Synechocystis sp. PCC 6803 led us to conclude that Suc-phosphate synthase (SPS) and Suc-phosphate phosphatase (SPP) [enzymes involved in Suc biosynthesis], and Suc synthase (SuS) [enzyme involved in Suc degradation] are proteins with modular architectures that might have arisen from functional domains shuffled during evolution. In cyanobacteria, Suc was identified as the main compatible osmolyte in many fresh-water strains, and as a minor or transient part of the total compatible solute pool in more halotolerant strains that accumulate also other organic compounds. However, Suc net accumulation, which can be ascribed to an increase of the expression of Suc biosynthesis enzymes, is also accompanied by an enhancement in Suc degradation by SuS, either in filamentous or unicellular strains. Recently, we have also characterized SuS from unicellular strains, like Microcystis aeruginosa PCC 7806. In the present work we studied the presence of Suc metabolism in bloom-forming cyanobacteria. In silico analyses revealed that putative SPS, SPP and SuS encoding genes (sps-like, spp-like and sus-like) are only present in a few bloom-forming strains. Among Nostocales and Stigonematales the distribution of genes related to Suc metabolism is ubiquitous, except for the strain Raphidiopsis brokii D9. Remarkably, among Chroococcales and Oscillatoriales sps- and spp-like sequences were only found in M. aeruginosa PCC 7806, being absent in other M. aeruginosa genomes, and in Leptolyngbya boryana PCC 6306, respectively. We functionally characterized SPS and SPP encoding genes from M. aeruginosa PCC 7806 and demonstrated that their expression is increased in response to a salt treatment. Moreover, the sus gene is located between the sps and spp with an intergenic distance of 160 and 6 bp, respectively, defining a transcriptional unit named Suc cluster (suc). Among all Suc-containing cyanobacteria whose genomes are fully sequenced to date, the gene organization of the Suc cluster present in M. aeruginosa PCC 7806 is unique. A global comparison of the genome in M. aeruginosa PCC 7806 (suc+) and the rest of the M. aeruginosa genomes (suc−) do not show the presence of syntenic regions. Our results and the cluster organization analysis of Suc metabolism genes led us to suggest that in the bloom-forming strains Suc genes might have been lost and later acquired by horizontal gene transfer from filamentous strains.