Plasticity of sucrose biosynthesis in bloom-forming cyanobacteria

KOLMAN, MA; SALERNO, G

St. Louis

Workshop; 11th Workshop on Cyanobacteria; 2013

International Center for Advanced Renewable Energy and Sustainability

Studies in cyanobacteria and the availability of complete genome sequences have significantly increased the knowledge of the structure of proteins involved in sucrose (Suc) metabolism, their origin and further evolution. The characterization of Suc biosynthesis-related enzymes (SPS, Suc-phosphate synthase and SPP, Suc-phosphate phosphatase) and the identification of their encoding genes in nitrogen-fixing filamentous strains and in Synechocystis sp. PCC 6803 led us to conclude that they are proteins with modular architecture that might have arisen from functional domains shuffled during evolution [1,2]. 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 [3,4]. However, Suc net accumulation, which can be ascribed to an increase of the expression of Suc biosynthesis enzymes, is accompanied also by an enhancement in Suc degradation by SuS (Suc synthase). Recently, we have characterized SuS in unicellular strains, like Microcystis aeruginosa PCC 7806 [5]. In the present work we studied the presence of Suc metabolism in bloom-forming cyanobacteria. In silico analyses of their genomes revealed that putative SPS and SPP encoding genes (sps-like and spp-like) are only present in a few bloom-forming cyanobacteria. Among Nostocales and Stigonematales the distribution of genes related to Suc metabolism is ubiquitous, except for the strain Raphidiopsis brokii D9. In contrast, among Chroococcales and Oscillatoriales sps-like 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. Firstly we functionally characterized SPS and SPP encoding genes (spsA and sppA) in M. aeruginosa PCC 7806 and demonstrated that their expressions are increased in response to a salt treatment. Moreover, since we found that the SuS gene (susA) is located between spsA and sppA with an intergenic distance of 160 and 6 bp, respectively, we define a Suc cluster organized as a transcriptional unit. Among all Suc-containing cyanobacteria, the gene organization of the Suc cluster in M. aeruginosa PCC 7806 is unique. A global comparison of M. aeruginosa PCC 7806 genome with those of other M. aeruginosa strains that lack the Suc cluster shows the absence of syntenic regions. Taken together our results and the cluster genome organization of Suc metabolism genes suggest that in the bloom-forming strains, Suc metabolism-related genes might have been lost and in some strains (like in PCC 7806) they have been acquired by horizontal gene transfer from filamentous nitrogen-fixing strains to constitute a Suc cluster. The driving force and/or the advantage of this acquisition is yet to be elucidated.