Cyanophage Trnas May Have a Role in Cross-Infectivity of Oceanic Prochlorococcus and Synechococcus Hosts

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Cyanophage Trnas May Have a Role in Cross-Infectivity of Oceanic Prochlorococcus and Synechococcus Hosts The ISME Journal (2012) 6, 619–628 & 2012 International Society for Microbial Ecology All rights reserved 1751-7362/12 www.nature.com/ismej ORIGINAL ARTICLE Cyanophage tRNAs may have a role in cross-infectivity of oceanic Prochlorococcus and Synechococcus hosts Hagay Enav, Oded Be´ja` and Yael Mandel-Gutfreund Faculty of Biology, Technion—Israel Institute of Technology, Haifa, Israel Marine cyanobacteria of the genera Prochlorococcus and Synechococcus are the most abundant photosynthetic prokaryotes in oceanic environments, and are key contributors to global CO2 fixation, chlorophyll biomass and primary production. Cyanophages, viruses infecting cyanobacter- ia, are a major force in the ecology of their hosts. These phages contribute greatly to cyanobacterial mortality, therefore acting as a powerful selective force upon their hosts. Phage reproduction is based on utilization of the host transcription and translation mechanisms; therefore, differences in the G þ C genomic content between cyanophages and their hosts could be a limiting factor for the translation of cyanophage genes. On the basis of comprehensive genomic analyses conducted in this study, we suggest that cyanophages of the Myoviridae family, which can infect both Prochlorococcus and Synechococcus, overcome this limitation by carrying additional sets of tRNAs in their genomes accommodating AT-rich codons. Whereas the tRNA genes are less needed when infecting their Prochlorococcus hosts, which possess a similar G þ C content to the cyanophage, the additional tRNAs may increase the overall translational efficiency of their genes when infecting a Synechococcus host (with high G þ C content), therefore potentially enabling the infection of multiple hosts. The ISME Journal (2012) 6, 619–628; doi:10.1038/ismej.2011.146; published online 20 October 2011 Subject Category: integrated genomics and post-genomics approaches in microbial ecology Keywords: codon usage; cross-infectivity; marine cyanophages; Prochlorococcus; Synechococcus; tRNA Introduction that phage genes would be adapted to optimal bacterial codons. On the basis of this assumption, Cyanobacteria of the Synechococcus and Prochloro- earlier studies have suggested that optimization of coccus genera are important contributors to photo- codon usage (CU) is a major force in phage–host synthetic productivity in the open oceans (Li et al., co-evolution (Krakauer and Jansen, 2002). Further, 1993; Liu et al., 1997; Partensky et al., 1999). in a comprehensive bioinformatics study, it has been Cyanophages, which are viruses infecting cyano- shown that generally the CU of bacteriophages is bacteria, belong to three morphologically defined strongly adapted to their specific host and differs families: Podoviridae, Siphoviridae and Myoviridae from the CU of other bacterial hosts (Bahir et al., (Suttle and Chan, 1993, 1994; Waterbury and Valois, 2009). Recently it has been reported that cyano- 1993; Wilson et al., 1993; Sullivan et al., 2003). phages, specifically myoviruses, carry up to 33 bona Among the cyanophages, podoviruses and sipho- fide tRNA genes in their genomes (Sullivan et al., viruses tend to be host-specific, whereas myoviruses 2010; Dreher et al., 2011). have a broader host range, even across genera Bailly-Bechet et al. (2007) proposed that tRNAs (Sullivan et al., 2003). Overall, myoviruses predo- carried in different phage genomes correspond to minate over other phage groups in different oceanic codons that are used highly by the phage genes but regions (Angly et al., 2006; DeLong et al., 2006). are rare in the host genome. In a recent study that Phages rely on host cellular mechanisms to tested CU adaptation in over 100 bacteriophages translate their proteins and reproduce. In order to infecting 10 different bacterial hosts, it was shown take advantage of the host tRNA pool, it is expected that bacteriophage genomes are under codon-selec- tive pressure imposed by the translational biases of their respective hosts (Carbone, 2008). On the other Correspondence: O Be´ja` or Y Mandel-Gutfreund, Faculty of hand, Weigele et al. (2007) proposed that tRNA Biology, Technion—Israel Institute of Technology, Haifa 32000, genes carried in viral genomes boost the expression Israel. E-mail: [email protected] or [email protected] of late phage genes encoding structural proteins. Received 24 March 2011; revised 6 September 2011; accepted 7 Interestingly, in the HIV-1 virus, which does not September 2011; published online 20 October 2011 carry tRNA genes in its genome, it was recently Role of cyanophage tRNAs in cross infectivty H Enav et al 620 shown that the tRNA-encoding codons, which are Relationship between phage genes and the host genome highly used by the virus but avoided by its host, are The CU profiles were calculated for each phage overrepresented in its virions (van Weringh et al., gene, as described above. Each phage gene was 2011). characterized by a vector representing the codon An intriguing conjecture is that phages carry frequencies observed for that gene. Cosine Similarity tRNA genes to enable cross-infectivity of hosts with Distance and tRCI (tRNA Relative Contribution different G þ C contents. In order to study this Index) were further calculated to compare the CU question, we used the unique cyanobacterial– profile of each gene with its host, as described cyanophage system where myophages (B35–40% below: G þ C) carry up to 33 different tRNA genes in their genomes (Sullivan et al., 2010; Dreher et al., 2011) Cosine similarity distance. Cosine similarity and can, in some cases, cross-infect different hosts distance is calculated using the formula with very different %G þ Ccontents(Prochlorococcus P64 B with 30–40% G þ C and marine Synechococcus pi à hi B with 50–60% G þ C) (Sullivan et al., 2003). Distance ¼ sffiffiffiffiffiffiffiffiffiffiffiffiffiffii¼1 s ffiffiffiffiffiffiffiffiffiffiffiffi ð2Þ P64 P64 2 2 pi à hi i¼1 i¼1 Materials and methods where pi is the frequency of codon i in the phage Data extraction and annotation gene and hi the frequency of codon i in the host Annotated genomes were downloaded from the genome. CAMERA website and the NCBI genome database. Information regarding cyanomyophages and their hosts was obtained from Sullivan et al. (2003) and tRCI calculation G Sabehi and D Lindell (personal communication). The tRCI was defined to estimate the potential gain Only phage–host pairs that had both the full in translational efficiency per phage gene when genomic sequence available and were annotated including phage tRNAs in the total tRNA pool. The were included in this work. A detailed list of all tRCI is based on the comparison between frequen- pairs of phages and hosts studied is given in cies of tRNA complementary codon (tCC) matching Supplementary Table S1. tRNA genes were anno- the phage tRNAs in the viral gene and the tCC in the tated using the tRNA-scanSE server (Lowe and host genome (see Equation (3)). Notably, the tRCI Eddy, 1997) with parameters set to default. index is calculated uniquely for each gene relative to a specific host (namely, the same gene in a given genome might have different tRCI values when infecting different hosts). CU and nucleotide usage (NU) profiles X f ðphage geneÞ CU and NU profiles were calculated for each tRCI ¼ log tCC ð3Þ organism using all protein-coding genes in the ftCCðhost genomeÞ genome. The CU for each codon was calculated as where ftcc is the frequency of tCC. the frequency of the given codon in a window of 1000 codons. Euclidean Distances (ED) between the CU and NU profiles of all genomes studied were Ranking the phage genes based on codon adaptation calculated as defined in Equation (1). ED values Ranking the phage genes according to the cosine were normalized from 0 to 1, representing the distance between the CU profile. For each host– highest to the lowest similarity, respectively. phage interaction pair, the phage genes were sorted Hierarchical clustering was performed using MeV based on the cosine distance between the vectors software (Saeed et al., 2006). vffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi representing their CU profile of the gene and the u CU profile of the specific host. The analysis was uX64 qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi t 2 repeated for all host–phage pairs. ED ¼ ðpi À hiÞ ð1Þ i¼1 Ranking the phage genes according to tRCI where pi is the frequency of codon i in the phage values. Following the calculation of tRCI of phage genome and hi the frequency of codon i in the host genes for each phage–host interaction, all genes in genome. the phage genomes were sorted and ranked accord- Codon Adaptation Index (CAI) values were calcu- ing to the tRCI calculated for a specific host. lated for each bacterial gene using the CAIcal server (Puigbo et al., 2008). CAI values for the genes in each genome were calculated relative to the CU table Detecting gene enrichment among the sorted phage genes representing the codon frequencies of the genes Each sorted list (either sorted according to cosine encoding ribosomal proteins or the codes for related distance or tRCI values) was divided into 10 ribosomal function in the corresponding genome. subgroups (bins) with an equal number of genes The ISME Journal Role of cyanophage tRNAs in cross infectivty H Enav et al 621 per bin. Bins were sorted according to the rank of the the codon bias of a gene relative to the bias of a set of genes, that is, bin #1 had the highest ranked genes highly expressed genes (Sharp and Li, 1987). In most and bin #10 the lowest ranked genes. The content of organisms, the set of highly expressed genes is each bin was analyzed to detect functional enrich- composed mostly of ribosomal protein-encoding ment using the hypergeometric distribution prob- genes. However, it is difficult to determine accu- ability (Equation (4)): p(x)4X defining enrichment rately an optimal gene set representing the codons of a specific gene function within a given bin, and that are favored in the selective process.
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