Evolution of translational elongation factor (EF) sequences: reliability of global phylogenies inferred from EF-1 alpha(Tu) and EF-2(G) proteins.

Creti, Roberta; Ceccarelli, Elena; Bocchetta, Maurizio; Sanangelantoni, Anna Maria; Tiboni, Orsola; Palm, Peter; Cammarano, Piero

doi:10.1073/pnas.91.8.3255

Cited by 44 publications

(30 citation statements)

References 45 publications

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“…This result is consistent with the previous observation that B. subtilis EF-G binds to 4.5S RNA from both E. coli and Clostridium perfringens (Shibata et al 1996). Interestingly, the sequence conservation between the archaeal and bacterial proteins is only ∼30%, with the highest conservation in the G domain responsible for GTP binding and hydrolysis (Cammarano et al 1992;Creti et al 1994;Thomas and Cavicchioli 1998). In contrast, the sequence of domain IV of 4.5S RNA is highly conserved in all three kingdoms of life, supporting the idea that this part of the RNA arose early in evolution, and that its sequence is constrained by multiple interacting factors.…”

Section: Discussionsupporting

confidence: 81%

Conserved but nonessential interaction of SRP RNA with translation factor EF-G

Sagar

Lucast²,

Doudna³

2004

RNA

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ABSTRACT4.5S RNA is essential for viability of Escherichia coli, and forms a key component of the signal recognition particle (SRP), a ubiquitous ribonucleoprotein complex responsible for cotranslational targeting of secretory proteins. 4.5S RNA also binds independently to elongation factor G (EF-G), a five-domain GTPase that catalyzes the translocation step during protein biosynthesis on the ribosome. Point mutations in EF-G suppress deleterious effects of 4.5S RNA depletion, as do mutations in the EF-G binding site within ribosomal RNA, suggesting that 4.5S RNA might play a critical role in ribosome function in addition to its role in SRP. Here we show that 4.5S RNA and EF-G form a phylogenetically conserved, low-affinity but highly specific complex involving sequence elements required for 4.5S binding to its cognate SRP protein, Ffh. Mutational analysis indicates that the same molecular structure of 4.5S RNA is recognized in each case. Surprisingly, however, the suppressor mutant forms of EF-G bind very weakly or undetectably to 4.5S RNA, implying that cells can survive 4.5S RNA depletion by decreasing the affinity between 4.5S RNA and the translational machinery. These data suggest that SRP function is the essential role of 4.5S RNA in bacteria.

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Section: Discussionsupporting

confidence: 81%

Conserved but nonessential interaction of SRP RNA with translation factor EF-G

Sagar

Lucast²,

Doudna³

2004

RNA

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“…In addition, the ribosome data have been criticized as artifactual (13) and are further challenged by the presence of "eocyte-specific characters" in two taxa now known to be euryarchaeotes (Thermoplasma and Thermococcus; refs. [5][6][7][8][9]. Our results with a combined EF-Tu/EF-G data set strongly reject both the original and rerooted (14) forms of the photocyte hypothesis, but they support the sisterhood of crenarchaeotes and eukaryotes.…”

supporting

confidence: 60%

“…3), as do almost all other relevant molecular phylogenetic data (5)(6)(7)(8)(9). Thus, the photocyte hypothesis, which postulates paraphyletic euryarchaeotes in either its original (11) or rerooted (14) form, can be soundly rejected.…”

Section: Discussionmentioning

confidence: 98%

“…Most data argue for a monophyletic Archaea composed of two kingdoms, crenarchaeotes and euryarchaeotes, with eukaryotes and eubacteria each arising separately (5)(6)(7)(8)(9). However, Lake et al (10,11) have argued for a polyphyletic Archaea, with a paraphyletic Euryarchaeota giving rise to eubacteria (the photocyte hypothesis) and a monophyletic Crenarchaeota arising with eukaryotes (the eocyte hypothesis).…”

mentioning

confidence: 99%

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The root of the universal tree and the origin of eukaryotes based on elongation factor phylogeny.

Baldauf

Palmer

Doolittle

1996

Proc. Natl. Acad. Sci. U.S.A.

257

157

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The genes for the protein synthesis elongation factors Tu (EF-Tu) and G (EF-G) are the products of an ancient gene duplication, which appears to predate the divergence of all extant organismal lineages. Thus, it should be possible to root a universal phylogeny based on either protein using the second protein as an outgroup. This approach was originally taken independently with two separate gene duplication pairs, (i) the regulatory and catalytic subunits of the proton ATPases and (ii) the protein synthesis elongation factors EF-Tu and EF-G. Questions about the orthology of the ATPase genes have obscured the former results, and the elongation factor data have been criticized for inadequate taxonomic representation and alignment errors. We have expanded the latter analysis using a broad representation of taxa from all three domains of life. All phylogenetic methods used strongly place the root of the universal tree between two highly distinct groups, the archaeons/eukaryotes and the eubacteria. We also find that a combined data set of EF-Tu and EF-G sequences favors placement of the eukaryotes within the Archaea, as the sister group to the Crenarchaeota. This relationship is supported by bootstrap values of 60-89% with various distance and maximum likelihood methods, while unweighted parsimony gives 58% support for archaeal monophyly.The use of primordially duplicated proteins to root the tree of life was pioneered by Gogarten et al. (1) for the catalytic and regulatory subunits of the V-and F-type ATPases and by Iwabe et al. (2) for the elongation factors Tu (EF-Tu) and G (EF-G). These analyses divide all living organisms into two clades, one consisting of the true bacteria, or eubacteria, and the other consisting of the archaeons and eukaryotes. The ATPase analyses are now complicated by the discoveries of eukaryotic/archaeal (V-type) ATPases in some eubacteria and of a eubacterial (F-type) ATPase in at least one archaebacterium, raising the possibility of multiple horizontal gene transfers (3). The elongation factor analyses have also been criticized, for the limited size of the homologous region, for alignment errors, and for inadequate taxonomic sampling [two eukaryotes, two eubacteria, and one archaebacterium for EF-G; and a few additional animal/fungal and organellar sequences for EF-Tu (4)].We have reanalyzed the elongation factor rooting with the much larger and more broadly representative data base now available for both proteins. This joint analysis now includes three to five representatives of each of the two archaeal kingdoms and a broad sampling of both eukaryotes and eubacteria. We have also modified and expanded the alignment of Iwabe et al. (2) using consensus sequences and crystal structures for both proteins. We find that rooted phylogenies for both elongation factors strongly support the Iwabe/ Gogarten rooting for the universal tree.These analyses address a second major issue, the origin of eukaryotes. Most data argue for a monophyletic Archaea composed of two kingdoms, crenarchaeotes ...

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“…In this context, phylogenetic analyses of inferred amino acid sequences of protein-encoding genes may be useful for resolving phylogenetic affiliation of this divergent and novel marine archaeal group. EF2 sequences are found in all cellular organisms, are highly conserved, and have proven particularly useful for constructing global phylogenies (5,6,19). Analyses of the EF2-encoding sequence on fosmid 4B7 (Fig.…”

Section: Discussionmentioning

confidence: 99%

Characterization of uncultivated prokaryotes: isolation and analysis of a 40-kilobase-pair genome fragment from a planktonic marine archaeon

et al. 1996

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One potential approach for characterizing uncultivated prokaryotes from natural assemblages involves genomic analysis of DNA fragments retrieved directly from naturally occurring microbial biomass. In this study, we sought to isolate large genomic fragments from a widely distributed and relatively abundant but as yet uncultivated group of prokaryotes, the planktonic marine Archaea. A fosmid DNA library was prepared from a marine picoplankton assemblage collected at a depth of 200 m in the eastern North Pacific. We identified a 38.5-kbp recombinant fosmid clone which contained an archaeal small subunit ribosomal DNA gene. Phylogenetic analyses of the small subunit rRNA sequence demonstrated its close relationship to that of previously described planktonic archaea, which form a coherent group rooted deeply within the Crenarchaeota branch of the domain Archaea. Random shotgun sequencing of subcloned fragments of the archaeal fosmid clone revealed several genes which bore highest similarity to archaeal homologs, including large subunit ribosomal DNA and translation elongation factor 2 (EF2). Analyses of the inferred amino acid sequence of archaeoplankton EF2 supported its affiliation with the Crenarchaeote subdivision of Archaea. Two gene fragments encoding proteins not previously found in Archaea were also identified: RNA helicase, responsible for the ATP-dependent alteration of RNA secondary structure, and glutamate semialdehyde aminotransferase, an enzyme involved in initial steps of heme biosynthesis. In total, our results indicate that genomic analysis of large DNA fragments retrieved from mixed microbial assemblages can provide useful perspective on the physiological potential of abundant but as yet uncultivated prokaryotes.Characterization of complex microbial communities by isolation and analysis of phylogenetically informative gene sequences has been an exciting development in microbiology (27,32). Studies using molecular phylogenetic approaches based on small subunit (ssu) rRNA sequence analyses have resulted in new estimates of the phylogenetic diversity contained within naturally occurring microbial assemblages. Entirely new phylogenetic lineages, which may sometimes represent major constituents of natural microbial communities, have been revealed by using such approaches (3,4,7,13,16,22,29). Although results of these studies have contributed substantially to assessments of naturally occurring microbial diversity, their utility as predictors of the physiological attributes of newly described phylotypes has been more limited. This is partly because many phylogenetically coherent prokaryote lineages, for example, the proteobacteria, often encompass a bewildering array of physiological and metabolic diversity. The problem is further complicated by the fact that many of the newly discovered phylotypes revealed by molecular phylogenetic analysis are proving difficult to enrich and isolate in pure culture. These limitations suggest the need for alternative approaches to characterize the physiological and metab...

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Evolution of translational elongation factor (EF) sequences: reliability of global phylogenies inferred from EF-1 alpha(Tu) and EF-2(G) proteins.

Cited by 44 publications

References 45 publications

Conserved but nonessential interaction of SRP RNA with translation factor EF-G

Conserved but nonessential interaction of SRP RNA with translation factor EF-G

The root of the universal tree and the origin of eukaryotes based on elongation factor phylogeny.

Characterization of uncultivated prokaryotes: isolation and analysis of a 40-kilobase-pair genome fragment from a planktonic marine archaeon

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