Genome reduction by deletion of paralogs in the marine cyanobacterium Prochlorococcus

Abstract

Several isolates of the marine cyanobacterial genus Prochlorococcus have smaller genome sizes than those of the closely related genus Synechococcus. In order to test whether loss of protein-coding genes has contributed to genome size reduction in Prochlorococcus, we reconstructed events of gene family evolution over a strongly supported phylogeny of 12 Prochlorococcus genomes and 9 Synechococcus genomes. Significantly, more events both of loss of paralogs within gene families and of loss of entire gene families occurred in Prochlorococcus than in Synechococcus. The number of nonancestral gene families in genomes of both genera was positively correlated with the extent of genomic islands (GIs), consistent with the hypothesis that horizontal gene transfer (HGT) is associated with GIs. However, even when only isolates with comparable extents of GIs were compared, significantly more events of gene family loss and of paralog loss were seen in Prochlorococcus than in Synechococcus, implying that HGT is not the primary reason for the genome size difference between the two genera.

FIG. 1.

ML tree (topology only) of Prochlorococcus (P.) and Synechococcus (S.) genomes used in analyses. Numbers on the branches represent the percentage of 100 bootstrap samples supporting the branch.

FIG. 2.

Numbers of reconstructed events of gain (+) and loss (-) of entire gene families in the ingroup phylogeny (based on fig. 1). “Boxes” indicate branches on which losses exceed gains.

FIG. 3.

Numbers of reconstructed events of gain (+) and loss (-) of paralogs in gene families in the ingroup phylogeny (based on fig. 1). Boxes indicate branches on which losses exceed gains.

FIG. 4.

(A) Relationship between number of paralogs lost within families and number of families lost in phylogeny of Prochlorococcus (solid circles) and Synechococcus (open circles); r = 0.900; P < 0.001. (B) Relationship between the number of ingroup-specific families and GI length in Prochlorococcus (solid circles) and Synechococcus (open circles); r = 0.741; P = 0.001.