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. 2004 Jul 27;101(30):11013-8.
doi: 10.1073/pnas.0401526101. Epub 2004 Jul 15.

Transfer of photosynthesis genes to and from Prochlorococcus viruses

Debbie Lindell  1 , Matthew B Sullivan, Zackary I Johnson, Andrew C Tolonen, Forest Rohwer, Sallie W Chisholm
Affiliations

Transfer of photosynthesis genes to and from Prochlorococcus viruses

Debbie Lindell et al. Proc Natl Acad Sci U S A. .

Abstract

Comparative genomics gives us a new window into phage-host interactions and their evolutionary implications. Here we report the presence of genes central to oxygenic photosynthesis in the genomes of three phages from two viral families (Myoviridae and Podoviridae) that infect the marine cyanobacterium Prochlorococcus. The genes that encode the photosystem II core reaction center protein D1 (psbA), and a high-light-inducible protein (HLIP) (hli) are present in all three genomes. Both myoviruses contain additional hli gene types, and one of them encodes the second photosystem II core reaction center protein D2 (psbD), whereas the other encodes the photosynthetic electron transport proteins plastocyanin (petE) and ferredoxin (petF). These uninterrupted, full-length genes are conserved in their amino acid sequence, suggesting that they encode functional proteins that may help maintain photosynthetic activity during infection. Phylogenetic analyses show that phage D1, D2, and HLIP proteins cluster with those from Prochlorococcus, indicating that they are of cyanobacterial origin. Their distribution among several Prochlorococcus clades further suggests that the genes encoding these proteins were transferred from host to phage multiple times. Phage HLIPs cluster with multicopy types found exclusively in Prochlorocococus, suggesting that phage may be mediating the expansion of the hli gene family by transferring these genes back to their hosts after a period of evolution in the phage. These gene transfers are likely to play a role in the fitness landscape of hosts and phages in the surface oceans.

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Figures

Fig. 1.
Fig. 1.
Arrangement of photosynthesis genes in three Prochlorococcus phages. (A) Podovirus P-SSP7. (B) Myovirus P-SSM2. (C) Myovirus P-SSM4. Black bars indicate genes related to photosynthesis, gray bars indicate genes commonly found in phage, and white bars indicate predicted ORFs of unknown function. Genes and their protein designations are as follows: psbA, D1; psbD, D2; hli, HLIP; petE, plastocyanin; petF, ferredoxin; 8, T7-like head-to-tail connector; 9, T7-like capsid assembly protein; 10, T7-like capsid protein; nrdB, T4-like ribonucleotide reductase β-subunit; 49, T4-like restriction endonuclease VII; and td, T4-like thymidylate synthetase.
Fig. 2.
Fig. 2.
Distance trees of PSII core reaction center proteins. (A) D1 (psbA). (B) D2 (psbD). Phage sequences are shown in bold. The host strains that each phage infects are indicated by black squares. Trees were generated from 244 and 336 amino acids for D1 and D2, respectively (see Figs. 4 and 5). Bootstrap values for distance and maximum parsimony analyses and quartet puzzling values for maximum likelihood analysis >50% are shown at the nodes (distance/maximum likelihood/maximum parsimony). Trees were rooted with Arabidopsis thaliana proteins. Essentially, the same topology was obtained when nucleotide trees (third position excluded) were constructed, except for psbA from P-SSP7, which clustered with HL Prochlorococcus, albeit with low bootstrap support. Pro, Prochlorococcus; Syn, Synechococcus; Anab, Anabaena; Syncy, Synechocystis.
Fig. 3.
Fig. 3.
Distance tree of HLIPs. Phage HLIPs appear in bold. The tree was generated from 36 amino acids (see Fig. 8), with gaps treated as missing data. generage clusters are indicated to the right of the tree, with cluster designations following ref. . Three discrepancies found between generage and distance tree clustering are indicated by the dashed line and their GR cluster designations. Asterisks denote proteins encoding at least six of the nine amino acids of the C-terminal 9-aa consensus sequence. Bootstrap and quartet puzzling values >50% are shown at the nodes for distance and maximum likelihood analyses, respectively. The tree was rooted with the single HLIP from A. thaliana. Abbreviations are as for Fig. 2.
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