Genome sequence of Synechococcus CC9311: Insights into adaptation to a coastal environment

Abstract

Coastal aquatic environments are typically more highly productive and dynamic than open ocean ones. Despite these differences, cyanobacteria from the genus Synechococcus are important primary producers in both types of ecosystems. We have found that the genome of a coastal cyanobacterium, Synechococcus sp. strain CC9311, has significant differences from an open ocean strain, Synechococcus sp. strain WH8102, and these are consistent with the differences between their respective environments. CC9311 has a greater capacity to sense and respond to changes in its (coastal) environment. It has a much larger capacity to transport, store, use, or export metals, especially iron and copper. In contrast, phosphate acquisition seems less important, consistent with the higher concentration of phosphate in coastal environments. CC9311 is predicted to have differences in its outer membrane lipopolysaccharide, and this may be characteristic of the speciation of some cyanobacterial groups. In addition, the types of potentially horizontally transferred genes are markedly different between the coastal and open ocean genomes and suggest a more prominent role for phages in horizontal gene transfer in oligotrophic environments.

Fig. 1.

Circular representation of the Synechococcus CC9311 overall genome structure. The outer scale designates coordinates in base pairs. The first circle shows predicted coding regions on the plus strand, color coded by role categories: violet, amino acid biosynthesis; light blue, biosynthesis of cofactors, prosthetic groups, and carriers; light green, cell envelope; red, cellular processes; brown, central intermediary metabolism; yellow, DNA metabolism; light gray, energy metabolism; magenta, fatty acid, and phospholipid metabolism; pink, protein synthesis and fate; orange, purines, pyrimidines, nucleosides, and nucleotides; olive, regulatory functions and signal transduction; dark green, transcription; teal, transport, and binding proteins; gray, unknown function; salmon, other categories; and blue, hypothetical proteins. The second circle shows predicted coding regions on the minus strand color coded by role categories. The third circle shows in red the set of 1,730 genes conserved between Synechococcus CC9311 and WH8102, the fourth circle shows percentage G+C in relation to the mean G+C in a 2,000-bp window in black, and the fifth circle shows the trinucleotide composition in black.

Fig. 2.

Phylogenetic tree of sensor kinases from Synechococcus CC9311 (sync_xxxx), and WH8102 (SYNWxxxx), Prochlorococcus marinus MI9313 (PMTxxxx), MED4 (PMMxxxx), and SS120 (Proxxxx). This maximum-likelihood phylogenetic tree was generated by using PHYLIP, and bootstrap values are indicated next to the branch nodes. Orthologous clusters conserved in all of the cyanobacteria shown are highlighted by lines on the side, the phosphate sensor is labeled, and the divergent sensors unique to CC9311 are highlighted with asterisks.

Fig. 3.

Overview of metal transport and metabolism in Synechococcus CC9311 and WH8102. Metal ion transporters are shown in the membrane, with the arrows indicating the direction of transport. Metal-binding proteins and metalloenzymes are shown inside the cell, and the number of copies of each system is shown in parentheses or within the protein. The color shading of the proteins indicates their distribution: magenta, present in both WH8102 and CC9311; red, present only in CC9311; and blue, present only in WH8102. Hatching indicates that the gene is located in a region with atypical trinucleotide content.