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Comparative Study
. 2007;8(12):R259.
doi: 10.1186/gb-2007-8-12-r259.

Diversity and Evolution of Phycobilisomes in Marine Synechococcus Spp.: A Comparative Genomics Study

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Free PMC article
Comparative Study

Diversity and Evolution of Phycobilisomes in Marine Synechococcus Spp.: A Comparative Genomics Study

Christophe Six et al. Genome Biol. .
Free PMC article

Abstract

Background: Marine Synechococcus owe their specific vivid color (ranging from blue-green to orange) to their large extrinsic antenna complexes called phycobilisomes, comprising a central allophycocyanin core and rods of variable phycobiliprotein composition. Three major pigment types can be defined depending on the major phycobiliprotein found in the rods (phycocyanin, phycoerythrin I or phycoerythrin II). Among strains containing both phycoerythrins I and II, four subtypes can be distinguished based on the ratio of the two chromophores bound to these phycobiliproteins. Genomes of eleven marine Synechococcus strains recently became available with one to four strains per pigment type or subtype, allowing an unprecedented comparative genomics study of genes involved in phycobilisome metabolism.

Results: By carefully comparing the Synechococcus genomes, we have retrieved candidate genes potentially required for the synthesis of phycobiliproteins in each pigment type. This includes linker polypeptides, phycobilin lyases and a number of novel genes of uncharacterized function. Interestingly, strains belonging to a given pigment type have similar phycobilisome gene complements and organization, independent of the core genome phylogeny (as assessed using concatenated ribosomal proteins). While phylogenetic trees based on concatenated allophycocyanin protein sequences are congruent with the latter, those based on phycocyanin and phycoerythrin notably differ and match the Synechococcus pigment types.

Conclusion: We conclude that the phycobilisome core has likely evolved together with the core genome, while rods must have evolved independently, possibly by lateral transfer of phycobilisome rod genes or gene clusters between Synechococcus strains, either via viruses or by natural transformation, allowing rapid adaptation to a variety of light niches.

Figures

Figure 1
Figure 1
The diversity of pigment types among marine Synechococcus spp. (a) Photograph of representative cultured strains of the major pigment types (1-3) and subtypes (3a-c) of marine Synechococcus grown under low white light and (b) corresponding absorption properties of whole cells. Pigment subtype 3d corresponds to type IV chromatic adapters, which are able to modify their PBS pigmentation from subtype 3b when grown under white or green light to subtype 3c when grown under blue light. The different colors of stars in panel A are a code for the different pigment types.
Figure 2
Figure 2
Absorption (continuous line) and fluorescence (dotted line) properties of isolated PBP complexes. (a) C-PC (as in Synechococcus spp. RS9917, WH5701 and WH8018); (b) PEI-A* (as in Synechococcus spp. WH8018 and WH7805); (c) PEI-A (as in Synechococcus spp. WH7803, Almo03 and RS9912); (d) PEI-B (as in Synechococcus spp. WH8102, CC9605 and Oli31).
Figure 3
Figure 3
Absorption (continuous line) and fluorescence (dotted line) properties of the isolated PEII complexes. (a) PEII-A (as in Synechococcus sp. WH7803); (b) PEII-B (as in Synechococcus sp. RCC307); (c) PEII-C (as in Synechococcus spp. CC9605 and WH8102). Type IV chromatic adapters have a PEII-B under white or green light and a PEII-C under blue light [34].
Figure 4
Figure 4
Comparison of PBS rod gene regions of the different pigment types of marine Synechococcus. Rectangles above and below the lines have a length proportional to the size of ORFs and correspond to the forward and the reverse strand, respectively. In several genomes, the sense of the rod region was inversed so that the regions all appear in the same direction. For the group formed by the chromatic adapters and RCC307, a few variations can be found with regard to the region shown here, which corresponds to BL107. First, the lyase-encoding gene(s) located near the 3'-end can either be a rpcE-F operon or rpcG, a pecEF-like fusion gene (see text). Second, the gene organization at the 5'-end can vary: unk1 is located elsewhere in the genome of RCC307 and the gene following unk2 is either the lyase gene cpcT in RS9916 and RCC307, unk3 in BL107 and CC9902, or none of these in CC9311. Colored stars indicate the pigment type of each strain (see Figure 1 for color code).
Figure 5
Figure 5
Coomassie blue stained LiDS polyacrylamide gradient (10-20%) gel of PBS linkers run using a Tris-glycine buffer system (left). A Tris-tricine buffer (right) gave higher band resolution for RCC307 and WH7803. Green dots indicate linker polypeptides fluorescing green under UV light due to the presence of a PUB chromophore. Colored stars indicate the pigment type of each strain (see Figure 1 for color code). FNR: ferredoxin:NADP+ oxidoreductase.
Figure 6
Figure 6
ML trees made with concatenated amino acid sequences of (a) all 51 ribosomal proteins (6,754 amino acid positions), (b) the AP proteins ApcA-B-C-D-F (710 amino acid positions), (c) the PC proteins CpcA-B or RpcA-B (332 amino acid positions), (d) the PEI proteins CpeA-B-Y-Z (943 amino acid positions) and (e) the PEII proteins MpeA-B-Y and Unk7-8-9 (1,007 amino acid positions). The first four trees are rooted with corresponding proteins from the primitive, freshwater cyanobacterium Gloeobacter violaceus, taken as an outgroup. The PEII tree is unrooted since these proteins are specific for marine Synechococcus spp. Numbers at internal branches correspond to bootstrap values for 1,000 replicate trees obtained with ML/NJ/MP methods. Colored stars indicate the pigment type of each strain (see Figure 1 for color code).
Figure 7
Figure 7
Proposed models of PBS structure for the different Synechococcus pigment types and subtypes. PBS cores are generally composed of three cylinders, but in some chromatic adapters possessing an extended LCM, it is likely composed of two additional half cylinders (see, for example, [58]). In pigment type 1, rods are composed of C-PC only; in pigment type 2, rods are composed of either C-PC, or R-PCIII and a PEI-like phycobiliprotein; in pigment type 3, rods comprise R-PC and two PE types (PEI and PEII). Cells of the latter pigment type bind PEB and PUB at a low (3a), medium (3b), high (3c) or variable (3d or type IV chromatic adapter) ratio. Colored stars indicate the pigment type of each strain (see Figure 1 for color code).

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