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Evolution of the Translocation and Assembly Module (TAM).

Heinz E, Selkrig J, Belousoff MJ, Lithgow T - Genome Biol Evol (2015)

Bottom Line: We report that TamA and a closely related protein TamL are confined almost exclusively to Proteobacteria and Bacteroidetes/Chlorobi respectively, whereas TamB is widely distributed across the majority of Gram-negative bacterial lineages.Several sequence characteristics were discovered to define the TamB protein family: A signal-anchor linkage to the inner membrane, beta-helical structure, conserved domain architecture and a C-terminal region that mimics outer membrane protein beta-strands.Taken together, the structural and phylogenetic analyses suggest that the TAM likely evolved from an original combination of BamA and TamB, with a later gene duplication event of BamA, giving rise to an additional Omp85 sequence that evolved to be TamA in Proteobacteria and TamL in Bacteroidetes/Chlorobi.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology, Monash University, Melbourne, Victoria, Australia.

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The evolution of the TAM operon. The left panel shows transcriptional units of tamB homologs as given in the BioCyc database collection (Caspi et al. 2014), the right panel highlights the presence or absence of an Omp85 protein in a putative operon with the respective TamB sequence. The orange dashed arrow indicates the likely HGT from the Alphaproteobacteria to a subgroup of Chlamydiae, as also seen in figure 6 and supplementary figure S9, Supplementary Material online; the orange/magenta dashed arrow indicates an HGT event of TamA from the ancestor of the Beta- and Gammaproteobacteria to the ancestor of the Bacteroidetes/Chlorobi, which acquired the lipid anchor and became TamL. Stars at the guidance tree reflect these two HGT events. For several genes, a gene encoding an Omp85 protein is present in the vicinity, but not in the same transcriptional unit. In the absence of experimental verification, these were interpreted as putative operons and are indicated by a dashed line separating the operons (left panel) and by round brackets surrounding the Omp85 protein icon (right panel). Protein icons enclosed by square brackets indicate the Omp85 protein most likely to interact with the respective TamB, but encoded elsewhere on the genome. The taxonomic guidance tree was derived as described for figure 3.
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evv097-F8: The evolution of the TAM operon. The left panel shows transcriptional units of tamB homologs as given in the BioCyc database collection (Caspi et al. 2014), the right panel highlights the presence or absence of an Omp85 protein in a putative operon with the respective TamB sequence. The orange dashed arrow indicates the likely HGT from the Alphaproteobacteria to a subgroup of Chlamydiae, as also seen in figure 6 and supplementary figure S9, Supplementary Material online; the orange/magenta dashed arrow indicates an HGT event of TamA from the ancestor of the Beta- and Gammaproteobacteria to the ancestor of the Bacteroidetes/Chlorobi, which acquired the lipid anchor and became TamL. Stars at the guidance tree reflect these two HGT events. For several genes, a gene encoding an Omp85 protein is present in the vicinity, but not in the same transcriptional unit. In the absence of experimental verification, these were interpreted as putative operons and are indicated by a dashed line separating the operons (left panel) and by round brackets surrounding the Omp85 protein icon (right panel). Protein icons enclosed by square brackets indicate the Omp85 protein most likely to interact with the respective TamB, but encoded elsewhere on the genome. The taxonomic guidance tree was derived as described for figure 3.

Mentions: Phylogenetic analysis of TamB revealed no clear correlation of the TamB proteins with respect to their presence in an operon with an Omp85 protein besides the monophyletic origin of the sequences associated with TamA or TamL (fig. 6 and supplementary fig. S8, Supplementary Material online). The chlamydial TamA–TamB operon seems to be derived through horizontal gene transfer (HGT) from the Alphaproteobacteria; this is also supported in the analysis of the Omp85 proteins (fig. 7 and supplementary fig. S9, Supplementary Material online). Although the Proteobacteria TamB forms a large monophyletic cluster (with the Chlamydiae; fig. 6 and supplementary fig. S8, Supplementary Material online), several Deltaproteobacteria and Epsilonproteobacteria cluster with the early-branching Phyla (such as Fusobacteria and Bacteroidetes); this likely HGT event is also reflected in the Omp85 sequences (Heinz and Lithgow 2014; fig. 7 and supplementary fig. S9, Supplementary Material online). The Acidobacteria and Aquificae both encode a second copy of BamA, which branches off monophyletic with TamA, indicating this to be the putative origin of the TAM (figs. 7 and 8 and supplementary fig. S9, Supplementary Material online). A consistent clustering of the early-branching Phyla including Spirochaetes, Deinococcus-Thermus, Firmicutes, and Cyanobacteria was also observed for TamB.Fig. 6.—


Evolution of the Translocation and Assembly Module (TAM).

Heinz E, Selkrig J, Belousoff MJ, Lithgow T - Genome Biol Evol (2015)

The evolution of the TAM operon. The left panel shows transcriptional units of tamB homologs as given in the BioCyc database collection (Caspi et al. 2014), the right panel highlights the presence or absence of an Omp85 protein in a putative operon with the respective TamB sequence. The orange dashed arrow indicates the likely HGT from the Alphaproteobacteria to a subgroup of Chlamydiae, as also seen in figure 6 and supplementary figure S9, Supplementary Material online; the orange/magenta dashed arrow indicates an HGT event of TamA from the ancestor of the Beta- and Gammaproteobacteria to the ancestor of the Bacteroidetes/Chlorobi, which acquired the lipid anchor and became TamL. Stars at the guidance tree reflect these two HGT events. For several genes, a gene encoding an Omp85 protein is present in the vicinity, but not in the same transcriptional unit. In the absence of experimental verification, these were interpreted as putative operons and are indicated by a dashed line separating the operons (left panel) and by round brackets surrounding the Omp85 protein icon (right panel). Protein icons enclosed by square brackets indicate the Omp85 protein most likely to interact with the respective TamB, but encoded elsewhere on the genome. The taxonomic guidance tree was derived as described for figure 3.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4494059&req=5

evv097-F8: The evolution of the TAM operon. The left panel shows transcriptional units of tamB homologs as given in the BioCyc database collection (Caspi et al. 2014), the right panel highlights the presence or absence of an Omp85 protein in a putative operon with the respective TamB sequence. The orange dashed arrow indicates the likely HGT from the Alphaproteobacteria to a subgroup of Chlamydiae, as also seen in figure 6 and supplementary figure S9, Supplementary Material online; the orange/magenta dashed arrow indicates an HGT event of TamA from the ancestor of the Beta- and Gammaproteobacteria to the ancestor of the Bacteroidetes/Chlorobi, which acquired the lipid anchor and became TamL. Stars at the guidance tree reflect these two HGT events. For several genes, a gene encoding an Omp85 protein is present in the vicinity, but not in the same transcriptional unit. In the absence of experimental verification, these were interpreted as putative operons and are indicated by a dashed line separating the operons (left panel) and by round brackets surrounding the Omp85 protein icon (right panel). Protein icons enclosed by square brackets indicate the Omp85 protein most likely to interact with the respective TamB, but encoded elsewhere on the genome. The taxonomic guidance tree was derived as described for figure 3.
Mentions: Phylogenetic analysis of TamB revealed no clear correlation of the TamB proteins with respect to their presence in an operon with an Omp85 protein besides the monophyletic origin of the sequences associated with TamA or TamL (fig. 6 and supplementary fig. S8, Supplementary Material online). The chlamydial TamA–TamB operon seems to be derived through horizontal gene transfer (HGT) from the Alphaproteobacteria; this is also supported in the analysis of the Omp85 proteins (fig. 7 and supplementary fig. S9, Supplementary Material online). Although the Proteobacteria TamB forms a large monophyletic cluster (with the Chlamydiae; fig. 6 and supplementary fig. S8, Supplementary Material online), several Deltaproteobacteria and Epsilonproteobacteria cluster with the early-branching Phyla (such as Fusobacteria and Bacteroidetes); this likely HGT event is also reflected in the Omp85 sequences (Heinz and Lithgow 2014; fig. 7 and supplementary fig. S9, Supplementary Material online). The Acidobacteria and Aquificae both encode a second copy of BamA, which branches off monophyletic with TamA, indicating this to be the putative origin of the TAM (figs. 7 and 8 and supplementary fig. S9, Supplementary Material online). A consistent clustering of the early-branching Phyla including Spirochaetes, Deinococcus-Thermus, Firmicutes, and Cyanobacteria was also observed for TamB.Fig. 6.—

Bottom Line: We report that TamA and a closely related protein TamL are confined almost exclusively to Proteobacteria and Bacteroidetes/Chlorobi respectively, whereas TamB is widely distributed across the majority of Gram-negative bacterial lineages.Several sequence characteristics were discovered to define the TamB protein family: A signal-anchor linkage to the inner membrane, beta-helical structure, conserved domain architecture and a C-terminal region that mimics outer membrane protein beta-strands.Taken together, the structural and phylogenetic analyses suggest that the TAM likely evolved from an original combination of BamA and TamB, with a later gene duplication event of BamA, giving rise to an additional Omp85 sequence that evolved to be TamA in Proteobacteria and TamL in Bacteroidetes/Chlorobi.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology, Monash University, Melbourne, Victoria, Australia.

Show MeSH
Related in: MedlinePlus