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Cited by 126RNA and protein synthesis mechanismsGenomics and Phylogenetic StudiesBacterial Genetics and Biotechnology

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Phylogenetic distribution of translational GTPases in bacteria

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Margus, Tõnu, Remm, Maido, Tenson, Tanel·2007·BMC Genomics
DOI 10.1186/1471-2164-8-15PMC PMC1780047
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Abstract

Background: Translational GTPases are a family of proteins in which GTPase activity is stimulated by the large ribosomal subunit. Conserved sequence features allow members of this family to be identified. Results: To achieve accurate protein identification and grouping we have developed a method combining searches with Hidden Markov Model profiles and tree based grouping. We found all the genes for translational GTPases in 191 fully sequenced bacterial genomes. The protein sequences were grouped into nine subfamilies. Analysis of the results shows that three translational GTPases, the translation factors EF-Tu, EF-G and IF2, are present in all organisms examined. In addition, several copies of the genes encoding EF-Tu and EF-G are present in some genomes. In the case of multiple genes for EF-Tu, the gene copies are nearly identical; in the case of multiple EF-G genes, the gene copies have been considerably diverged. The fourth translational GTPase, LepA, the function of which is currently unknown, is also nearly universally conserved in bacteria, being absent from only one organism out of the 191 analyzed. The translation regulator, TypA, is also present in most of the organisms examined, being absent only from bacteria with small genomes. Surprisingly, some of the well studied translational GTPases are present only in a very small number of bacteria. The translation termination factor RF3 is absent from many groups of bacteria with both small and large genomes. The specialized translation factor for selenocysteine incorporation – SelB – was found in only 39 organisms. Similarly, the tetracycline resistance proteins (Tet) are present only in a small number of species. Proteins of the CysN/NodQ subfamily have acquired functions in sulfur metabolism and production of signaling molecules. The genes coding for CysN/NodQ proteins were found in 74 genomes. This protein subfamily is not confined to Proteobacteria, as suggested previously but present also in many other groups of bacteria. Conclusion: Four of the translational GTPase subfamilies (IF2, EF-Tu, EF-G and LepA) are represented by at least one member in each bacterium studied, with one exception in LepA. This defines the set of translational GTPases essential for basic cell functions.

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Figures

Figure 1 Translational GTPase discovery and grouping flow chart.
Figure 1 Translational GTPase discovery and grouping flow chart.CC BY · PubMed Central
Figure 2 Some examples of frame-shifts (I) and alternative gene start positions (II) for genes marked as exceptions. The full list of exceptions is presented in Additional file 1.
Figure 2 Some examples of frame-shifts (I) and alternative gene start positions (II) for genes marked as exceptions. The full list of exceptions is presented in Additional file 1.CC BY · PubMed Central
Figure 3 Unrooted consensus tree of translational GTPases. Nine major groups are distinguished by high bootstrap values that are shown by numbers on roots of branches. Underlying multiple alignment is based on GTPase domain alignment made with HMMALIGN [18] against GTP_EFTU model from Pfam database. Tree is calculated using PROTDIST (using JTT matrix) [23], NEIGHBOR and CONSENSE (Extended Majority Rule) from the PHYLIP 3.62 package [23]. One hundred bootstraps were performed to evaluate branch reliability.
Figure 3 Unrooted consensus tree of translational GTPases. Nine major groups are distinguished by high bootstrap values that are shown by numbers on roots of branches. Underlying multiple alignment is based on GTPase domain alignment made with HMMALIGN [18] against GTP_EFTU model from Pfam database. Tree is calculated using PROTDIST (using JTT matrix) [23], NEIGHBOR and CONSENSE (Extended Majority Rule) from the PHYLIP 3.62 package [23]. One hundred bootstraps were performed to evaluate branch reliability.CC BY · PubMed Central
Figure 4 Phylogenetic distribution of translational GTPases. The number of genes in different trGTPase subfamilies is shown in the context of the 16S ribosomal RNA based phylogenetic tree (The bar indicates 0.1 PAM units). The genome sizes in millions of basepairs ("size") and rRNA operon copy numbers ("rRNA") are also shown. The symbol "a" indicates that the gene (or one of the genes, in case of multiple genes) might be translated using an alterative in-frame start codon (Fig. 2, see Additional file 1); the symbol "b" indicates that the gene (or one of the genes, in case of multiple genes) might be translated through a frame-shift event (Fig. 2, see Additional file 1). In the IF2 column the proteins containing only one IF2N domain are marked with "N". In the ATPS column the numbers indicate proteins of the CysN/NodQ subfamily (ATPS2). The CysN ("C") and NodQ ("Q") proteins are shown separately. For example, "1(C)2(Q)" indicates the presence of one CysN and two NodQ proteins. The ATPS1 family is marked with "*" ("**" indicates two proteins of this family).
Figure 4 Phylogenetic distribution of translational GTPases. The number of genes in different trGTPase subfamilies is shown in the context of the 16S ribosomal RNA based phylogenetic tree (The bar indicates 0.1 PAM units). The genome sizes in millions of basepairs ("size") and rRNA operon copy numbers ("rRNA") are also shown. The symbol "a" indicates that the gene (or one of the genes, in case of multiple genes) might be translated using an alterative in-frame start codon (Fig. 2, see Additional file 1); the symbol "b" indicates that the gene (or one of the genes, in case of multiple genes) might be translated through a frame-shift event (Fig. 2, see Additional file 1). In the IF2 column the proteins containing only one IF2N domain are marked with "N". In the ATPS column the numbers indicate proteins of the CysN/NodQ subfamily (ATPS2). The CysN ("C") and NodQ ("Q") proteins are shown separately. For example, "1(C)2(Q)" indicates the presence of one CysN and two NodQ proteins. The ATPS1 family is marked with "*" ("**" indicates two proteins of this family).CC BY · PubMed Central
Figure 5 Phylogenetic distribution of translational GTPases. The number of genes in different trGTPase subfamilies is shown in the context of the 16S ribosomal RNA based phylogenetic tree (The bar indicates 0.1 PAM units). The genome sizes in millions of basepairs ("size") and rRNA operon copy numbers ("rRNA") are also shown. The symbol "a" indicates that the gene (or one of the genes, in case of multiple genes) might be translated using an alterative in-frame start codon (Fig. 2, see Additional file 1); the symbol "b" indicates that the gene (or one of the genes, in case of multiple genes) might be translated through a frame-shift event (Fig. 2, see Additional file 1). In the IF2 column the proteins containing only one IF2N domain are marked with "N". In the ATPS column the numbers indicate proteins of the CysN/NodQ subfamily (ATPS2). The CysN ("C") and NodQ ("Q") proteins are shown separately. For example, "1(C)2(Q)" indicates the presence of one CysN and two NodQ proteins. The ATPS1 family is marked with "*" ("**" indicates two proteins of this family).
Figure 5 Phylogenetic distribution of translational GTPases. The number of genes in different trGTPase subfamilies is shown in the context of the 16S ribosomal RNA based phylogenetic tree (The bar indicates 0.1 PAM units). The genome sizes in millions of basepairs ("size") and rRNA operon copy numbers ("rRNA") are also shown. The symbol "a" indicates that the gene (or one of the genes, in case of multiple genes) might be translated using an alterative in-frame start codon (Fig. 2, see Additional file 1); the symbol "b" indicates that the gene (or one of the genes, in case of multiple genes) might be translated through a frame-shift event (Fig. 2, see Additional file 1). In the IF2 column the proteins containing only one IF2N domain are marked with "N". In the ATPS column the numbers indicate proteins of the CysN/NodQ subfamily (ATPS2). The CysN ("C") and NodQ ("Q") proteins are shown separately. For example, "1(C)2(Q)" indicates the presence of one CysN and two NodQ proteins. The ATPS1 family is marked with "*" ("**" indicates two proteins of this family).CC BY · PubMed Central
Figure 6 Phylogenetic distribution of translational GTPases. The number of genes in different trGTPase subfamilies is shown in the context of the 16S ribosomal RNA based phylogenetic tree (The bar indicates 0.1 PAM units). The genome sizes in millions of basepairs ("size") and rRNA operon copy numbers ("rRNA") are also shown. The symbol "a" indicates that the gene (or one of the genes, in case of multiple genes) might be translated using an alterative in-frame start codon (Fig. 2, see Additional file 1); the symbol "b" indicates that the gene (or one of the genes, in case of multiple genes) might be translated through a frame-shift event (Fig. 2, see Additional file 1). In the IF2 column the proteins containing only one IF2N domain are marked with "N". In the ATPS column the numbers indicate proteins of the CysN/NodQ subfamily (ATPS2). The CysN ("C") and NodQ ("Q") proteins are shown separately. For example, "1(C)2(Q)" indicates the presence of one CysN and two NodQ proteins. The ATPS1 family is marked with "*" ("**" indicates two proteins of this family).
Figure 6 Phylogenetic distribution of translational GTPases. The number of genes in different trGTPase subfamilies is shown in the context of the 16S ribosomal RNA based phylogenetic tree (The bar indicates 0.1 PAM units). The genome sizes in millions of basepairs ("size") and rRNA operon copy numbers ("rRNA") are also shown. The symbol "a" indicates that the gene (or one of the genes, in case of multiple genes) might be translated using an alterative in-frame start codon (Fig. 2, see Additional file 1); the symbol "b" indicates that the gene (or one of the genes, in case of multiple genes) might be translated through a frame-shift event (Fig. 2, see Additional file 1). In the IF2 column the proteins containing only one IF2N domain are marked with "N". In the ATPS column the numbers indicate proteins of the CysN/NodQ subfamily (ATPS2). The CysN ("C") and NodQ ("Q") proteins are shown separately. For example, "1(C)2(Q)" indicates the presence of one CysN and two NodQ proteins. The ATPS1 family is marked with "*" ("**" indicates two proteins of this family).CC BY · PubMed Central
Figure 7 The number of trGTPase subfamilies encoded in one genome presented in correlation with genome size. A sliding window with length 15 genomes was used to draw the trendline.
Figure 7 The number of trGTPase subfamilies encoded in one genome presented in correlation with genome size. A sliding window with length 15 genomes was used to draw the trendline.CC BY · PubMed Central
Figure 8 The number of gene copies in each subfamily presented in correlation with genome size. The ATPS proteins include both CysN/NodQ (ATPS2) and ATPS1. A sliding window with length 15 genomes was used to draw the trendline.
Figure 8 The number of gene copies in each subfamily presented in correlation with genome size. The ATPS proteins include both CysN/NodQ (ATPS2) and ATPS1. A sliding window with length 15 genomes was used to draw the trendline.CC BY · PubMed Central

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  1. Garrity GM Bell, J. A., Lilburn, T. G.: Taxonomic Outline of the Procaryotes. Bergey's Manual of Systematic Bacteriology, Second Edition. 2004, Springer-Verlag, 5:

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Metadata

Authors
Margus, T., Remm, M., & Tenson, T.
Affiliations
University of Tartu (EE)
Corresponding author
Tenson, Tanel
ORCID
Venue
BMC Genomics
Publisher
Springer Science and Business Media LLC
Published
2007-01-10
Volume
8
Issue
1
Pages
15-15
ISSN
1471-2164 (ISSN-L)
DOI
10.1186/1471-2164-8-15
PMC
PMC1780047
OpenAlex
W1939105798
Cited by
115
References
114
Citations by year
2026: 1 · 2025: 5 · 2024: 2 · 2023: 3 · 2022: 5 · 2021: 14 · 2020: 8 · 2019: 1 · 2018: 5 · 2017: 7 · 2016: 11 · 2015: 8 · 2014: 6 · 2013: 8 · 2012: 4
FWCI
2.51
Type
journal article
Language
en
Open access
Licence
Locations
  • BMC Genomics (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Wellcome Trust (070210)
  • Eesti Teadusfondi
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords
translational GTPases, bacterial phylogeny, elongation factor Tu, elongation factor G, initiation factor 2, Lepas, Rf3, Selb, selenocysteine incorporation, essential genes, gene family evolution
MeSH terms
Amino Acid Sequence, Bacteria, Base Sequence, DNA, Bacterial, Markov Chains, Molecular Sequence Data, Phylogeny, Sequence Homology, Nucleic Acid, Protein Biosynthesis, Genome, Bacterial, GTP Phosphohydrolases

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