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Direct Phylogenetic Evidence for Lateral Transfer of Elongation Factor-Like Gene

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Direct Phylogenetic Evidence for Lateral Transfer of Elongation Factor-Like Gene Direct phylogenetic evidence for lateral transfer of elongation factor-like gene Ryoma Kamikawa*, Yuji Inagaki†‡, and Yoshihiko Sako* *Laboratory of Marine Microbiology, Division of Applied Biosciences, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan; and †Center of Computational Sciences and Institute of Biological Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8577, Japan Edited by W. Ford Doolittle, Dalhousie University, Halifax, NS, Canada, and approved March 18, 2008 (received for review November 26, 2007) Genes encoding elongation factor-like (EFL) proteins, which show veys of EFL genes revealed that (i) ‘‘EFL-containing’’ lineages high similarity to elongation factor-1␣ (EF-1␣), have been found in are scattered amongst ‘‘EF-1␣-containing’’ lineages and (ii) phylogenetically distantly related eukaryotes. The sporadic distri- EF-1␣ and EFL genes are mutually exclusively distributed bution of ‘‘EFL-containing’’ lineages within ‘‘EF-1␣-containing’’ amongst eukaryotes (9–12). Such EF-1␣/EFL distribution can be lineages indirectly, but strongly, suggests lateral gene transfer as achieved by the lateral gene transfer (LGT) scenario assumes the principal driving force in EFL evolution. However, one of the that all eukaryotes primarily lacked EFL genes, and the EFL most critical aspects in the above hypothesis, the donor lineages in genes were separately spread into distantly related lineages via any putative cases of lateral EFL gene transfer, remained unclear. LGT. The exogenous EFL likely took over EF-1␣ functions, and In this study, we provide direct evidence for lateral transfer of an the endogenous EF-1␣ genes eventually disappeared from the EFL gene through the analyses of 10 diatom EFL genes. All diatom genomes. Alternatively, the ‘‘gene-loss’’ scenario, in which as- EFL homologues tightly clustered in phylogenetic analyses, sug- sumes that eukaryotes originally possessed both EF-1␣ and EFL gesting acquisition of the exogenous EFL gene early in diatom genes, is also possible. After divergence of major eukaryotic evolution. Our survey additionally identified Thalassiosira pseud- groups, the mosaic EF-1␣/EFL distribution could have been onana as a eukaryote bearing EF-1␣ and EFL genes and secondary created by multiple independent EFL (or EF-1␣) gene-loss EFL gene loss in Phaeodactylum tricornutum, the complete genome events. Although the current data cannot definitely distinguish ␣ of which encodes only the EF-1 gene. Most importantly, the EFL the evolutionary mode of EFL genes, the LGT scenario is EVOLUTION phylogeny recovered a robust grouping of homologues from generally preferred over the alternative scenario based on a diatoms, the cercozoan Bigelowiella natans, and the foraminifer parsimony-based argument. Because EFL-containing lineages Planoglabratella opecularis, with the diatoms nested within the are currently minor amongst eukaryotes, the number of events Bigelowiella plus Planoglabratella (Rhizaria) grouping. The partic- required for the LGT scenario is equal to or smaller than the ular relationships recovered are further consistent with two char- number of EFL-containing lineages. However, in the gene-loss acteristic sequence motifs. The best explanation of our data anal- scenario, all EF-1␣-containing lineages—presumably the major- yses is an EFL gene transfer from a foraminifer to a diatom, the first ity of eukaryotes—would have had to experience EFL gene loss. case in which the donor–recipient relationship was clarified. Fi- Thus, the number of events required in this scenario would be nally, based on a reverse transcriptase quantitative PCR assay and much larger than that required in the LGT scenario. Neverthe- the genome information of Thalassiosira and Phaeodactylum,we less, the LGT scenario for EFL evolution currently depends propose the loss of elongation factor function in Thalassiosira solely on the observed mosaic EF-1␣/EFL distribution (9–12). EF-1␣. For any putative cases of lateral EFL gene transfer, phylogenetic analyses always failed to unveil the donor lineages (9–12). To EF-1␣ ͉ EFL ͉ eukaryotic phylogeny achieve better understanding of EFL evolution, information regarding the donor lineages of EFL genes would be ␣ ␣ indispensable. ranslation elongation factor 1 (EF-1 ) and its eubacterial ␣ Torthologue, EF-Tu, have been considered as indispensable We here conducted a survey of EF-1 /EFL genes in 11 diatom proteins involved in the elongation step of protein synthesis (1, species. Although no EFL gene has been officially reported for 2). Because of the critical tasks of translation elongation factors, diatoms, we sequenced and/or identified 10 diatom EFL genes. it is widely believed that EF-1␣/EF-Tu genes have been vertically Our data analyses indicated that an EFL gene was established inherited from the last universal common ancestor (3–5), and the early in diatom evolution and that the pennate diatom Phae- gene products are ubiquitous in all extant cells. However, odactylum tricornutum secondarily lost. Of utmost interest is the large-scale sequence data from phylogenetically diverged organ- origin of diatom EFL genes. An EFL phylogeny recovered a isms started unveiling cases that clearly violate the above pre- strongly supported clade of the EFL homologues from the Bigelowiella natans Planoglabratella conception about EF-1␣/EF-Tu evolution. First, multiple cases cercozoan , the foraminifer opecularis, and diatoms, with the diatoms nested inside a ‘‘Rhi- of lateral EF-1␣/EF-Tu gene transfer are described in refs. 6–8. zarian’’ grouping. Characteristic sequence motifs in the EFL Second, the absolute ubiquity of EF-1␣ has also been called into alignment are congruous with this relationship, arguing against question. For instance, no EF-1␣ gene has been identified in the complete nuclear genome of the green alga Chlamydomonas reinhardtii (genome.jgi-psf.org). Instead, this organism possesses Author contributions: R.K., Y.I., and Y.S. designed research; R.K. and Y.I. performed the gene encoding an elongation factor-like (EFL) protein that research; R.K. and Y.I. analyzed data; and R.K., Y.I., and Y.S. wrote the paper. ␣ bears sequence similarity to, but is clearly divergent from, EF-1 The authors declare no conflict of interest. (9). An in silico analysis of functional divergence between This article is a PNAS Direct Submission. ␣ EF-1 and EFL suggested that EFL possesses at least a primary Data deposition: The sequences reported in this paper have been deposited in the Gen- EF-1␣ function, such as the catalysis of nascent peptide elon- Bank, European Molecular Biology Laboratory, and DNA Data Bank of Japan databases gation (9). (accession nos. AB368767–AB368774). Although EF-1␣ and EFL likely share the same cellular ‡To whom correspondence should be addressed. E-mail: [email protected]. function, the postulated evolutionary mode of transmission for This article contains supporting information online at www.pnas.org/cgi/content/full/ EFL genes is significantly different from that for EF-1␣ genes, 0711084105/DCSupplemental. which mainly comprises vertical gene inheritance. Recent sur- © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0711084105 PNAS ͉ May 13, 2008 ͉ vol. 105 ͉ no. 19 ͉ 6965–6969 Downloaded by guest on September 25, 2021 ABC Fig. 1. Phylogenetic relationship among EFL homologues. (A) Maximum-likelihood EFL phylogeny estimated by IQPNNI. Only bootstrap values Ն70% are indicated. The results from PhyML and MrBayes analyses are not shown, because those estimates were not significantly different from that from IQPNNI. The P nodes supported by Bayesian posterior probabilities Ն 0.95 are highlighted by dots. (B) The /TKK motif exclusively shared among the diatom and Planoglabratella EFL homologues. Gaps are represented by dashes. Possible secondary structures deduced from a yeast EF-1␣ tertiary structure (PDB ID code 1IJF) are shown above P the alignment. Helix and sheet are shown by cylinder and arrow, respectively. Because the secondary structure of the /TKK motif (and the corresponding region in other EFL homologues) is unclear, question marks are inserted. Numbers below the alignment are the amino acid positions in Tharassiosira pseudonana EFL, and those in parentheses are the corresponding positions in yeast EF-1␣.(C) K indel exclusively shared among the diatom, Planoglabratella, and Bigelowiella EFL homologues. Details are as described in B. phylogenetic artifact. Thus, both the tree topology and sequence Skeletonema costatum, and four pennate diatoms, Asterionella features suggest that an EFL gene was most likely transferred glacialis, Cylindrotheca closterium, Achnanthes kuwaitensis, and from a foraminifer to a diatom. To our knowledge, this is the first Thalassionema nitzchioides (Table 1). The initial survey was case whereby the donor of an EFL gene is clear, making it conducted by using sets of degenerate PCR primers designed for significant for a deeper understanding of EF-1␣/EFL evolution. amplifying short DNA fragments encoding the N termini of We also discussed a potential loss of elongation factor (EF) EF-1␣ and EF-1␣-related proteins (i.e., EFL, eukaryotic release functions in EF-1␣ of Thalassiosira, an organism using both factor 3, hsp70 subfamily B suppressor 1). Subsequent cloning EF-1␣ and EFL. and sequencing of the amplified fragments revealed that two or more than two EF-1␣/EF-1␣-related genes were amplified by a Results and Discussion single PCR for all species examined except Ditylum
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