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Evolutionary analysis of the ENTH/ANTH/VHS protein superfamily reveals a coevolution between membrane trafficking and metabolism.

De Craene JO, Ripp R, Lecompte O, Thompson JD, Poch O, Friant S - BMC Genomics (2012)

Bottom Line: Our in silico analysis of this ENTH/ANTH/VHS superfamily, consisting of proteins gathered from 84 complete genomes representative of the different eukaryotic taxa, revealed that genomic distribution of this superfamily allows to discriminate Fungi and Metazoa from Plantae and Protists.Next, in a four way genome wide comparison, we showed that this discriminative feature is observed not only for other membrane trafficking effectors, but also for proteins involved in metabolism and in cytokinesis, suggesting that metabolism, cytokinesis and intracellular trafficking pathways co-evolved.Moreover, some of the proteins identified were implicated in multiple functions, in either trafficking and metabolism or trafficking and cytokinesis, suggesting that membrane trafficking is central to this co-evolution process.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Molecular and Cellular Genetics, UMR7156 CNRS/Université de Strasbourg, 21 rue Descartes, 67084, Strasbourg, France.

ABSTRACT

Background: Membrane trafficking involves the complex regulation of proteins and lipids intracellular localization and is required for metabolic uptake, cell growth and development. Different trafficking pathways passing through the endosomes are coordinated by the ENTH/ANTH/VHS adaptor protein superfamily. The endosomes are crucial for eukaryotes since the acquisition of the endomembrane system was a central process in eukaryogenesis.

Results: Our in silico analysis of this ENTH/ANTH/VHS superfamily, consisting of proteins gathered from 84 complete genomes representative of the different eukaryotic taxa, revealed that genomic distribution of this superfamily allows to discriminate Fungi and Metazoa from Plantae and Protists. Next, in a four way genome wide comparison, we showed that this discriminative feature is observed not only for other membrane trafficking effectors, but also for proteins involved in metabolism and in cytokinesis, suggesting that metabolism, cytokinesis and intracellular trafficking pathways co-evolved. Moreover, some of the proteins identified were implicated in multiple functions, in either trafficking and metabolism or trafficking and cytokinesis, suggesting that membrane trafficking is central to this co-evolution process.

Conclusions: Our study suggests that membrane trafficking and compartmentalization were not only key features for the emergence of eukaryotic cells but also drove the separation of the eukaryotes in the different taxa.

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Phylogeny of the proteins with an ENTH, ANTH or VHS domain. Unrooted tree displaying the grouping of most ANTH, ENTH and VHS proteins from 42 fully sequenced organisms. The tree was generated using the highly conserved ∝-helices 2 to 7 of the N-terminal domain. (●) indicates branches with at least 70% confidence after 500 bootstrap calculations. Protein subfamilies are indicated by different colors.
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Figure 1: Phylogeny of the proteins with an ENTH, ANTH or VHS domain. Unrooted tree displaying the grouping of most ANTH, ENTH and VHS proteins from 42 fully sequenced organisms. The tree was generated using the highly conserved ∝-helices 2 to 7 of the N-terminal domain. (●) indicates branches with at least 70% confidence after 500 bootstrap calculations. Protein subfamilies are indicated by different colors.

Mentions: As the C-terminal parts of these proteins are highly divergent and frequently specific of each family or subfamily, a robust phylogenetic tree (see Material and Methods section) was calculated using the most conserved common region of the aligned proteins (between ∝-helices 2 and 7 of the N-terminal domain). The phylogenetic tree (Figure1) based on the conserved N-terminal domain shows a very similar clustering to the one obtained with the full-length proteins thus suggesting that the N- and C-terminal parts of ENTH/ANTH/VHS proteins have experienced concerted selective pressures during evolution. Broadly, Plantae proteins of the ANTH family (PICALM, ANTH subfamilies) and the VHS family (GGA, VHS, STAM, TOM subfamilies) clustered on a separate branch from Opisthokonta proteins. The ENTH subfamilies did not display such separation even though our phylogenetic tree confirmed that ENTHA-containing proteins were localized on a separate branch from the ENTHB-containing protein (Figure1) as previously described[17]. Indeed, most Plantae ENTHA subfamilies (ENTHA1,2,3) clustered among the Opisthokonta group and the last one (ENTHA4) clustered on a separate branch displaying a closer relationship with protist and some fungal proteins (ENTHC). Interestingly, the yeast Ent5 protein and its fungal homologues are members of the ENTH family. Due to its sequence divergence, the yeast Ent5 protein was described either as belonging to the ENTH or ANTH family[19,20]. Based on our extended MACS and the phylogenetic tree, it clearly stands out that this small group is clearly distinct from all other Fungal ANTH members which cluster together on one branch separated from ENTH members. This is in keeping with the in vivo function of the yeast Ent5 in Golgi and endosomal sorting, a function performed by members of the ENTHA subfamily[19,20].


Evolutionary analysis of the ENTH/ANTH/VHS protein superfamily reveals a coevolution between membrane trafficking and metabolism.

De Craene JO, Ripp R, Lecompte O, Thompson JD, Poch O, Friant S - BMC Genomics (2012)

Phylogeny of the proteins with an ENTH, ANTH or VHS domain. Unrooted tree displaying the grouping of most ANTH, ENTH and VHS proteins from 42 fully sequenced organisms. The tree was generated using the highly conserved ∝-helices 2 to 7 of the N-terminal domain. (●) indicates branches with at least 70% confidence after 500 bootstrap calculations. Protein subfamilies are indicated by different colors.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3473312&req=5

Figure 1: Phylogeny of the proteins with an ENTH, ANTH or VHS domain. Unrooted tree displaying the grouping of most ANTH, ENTH and VHS proteins from 42 fully sequenced organisms. The tree was generated using the highly conserved ∝-helices 2 to 7 of the N-terminal domain. (●) indicates branches with at least 70% confidence after 500 bootstrap calculations. Protein subfamilies are indicated by different colors.
Mentions: As the C-terminal parts of these proteins are highly divergent and frequently specific of each family or subfamily, a robust phylogenetic tree (see Material and Methods section) was calculated using the most conserved common region of the aligned proteins (between ∝-helices 2 and 7 of the N-terminal domain). The phylogenetic tree (Figure1) based on the conserved N-terminal domain shows a very similar clustering to the one obtained with the full-length proteins thus suggesting that the N- and C-terminal parts of ENTH/ANTH/VHS proteins have experienced concerted selective pressures during evolution. Broadly, Plantae proteins of the ANTH family (PICALM, ANTH subfamilies) and the VHS family (GGA, VHS, STAM, TOM subfamilies) clustered on a separate branch from Opisthokonta proteins. The ENTH subfamilies did not display such separation even though our phylogenetic tree confirmed that ENTHA-containing proteins were localized on a separate branch from the ENTHB-containing protein (Figure1) as previously described[17]. Indeed, most Plantae ENTHA subfamilies (ENTHA1,2,3) clustered among the Opisthokonta group and the last one (ENTHA4) clustered on a separate branch displaying a closer relationship with protist and some fungal proteins (ENTHC). Interestingly, the yeast Ent5 protein and its fungal homologues are members of the ENTH family. Due to its sequence divergence, the yeast Ent5 protein was described either as belonging to the ENTH or ANTH family[19,20]. Based on our extended MACS and the phylogenetic tree, it clearly stands out that this small group is clearly distinct from all other Fungal ANTH members which cluster together on one branch separated from ENTH members. This is in keeping with the in vivo function of the yeast Ent5 in Golgi and endosomal sorting, a function performed by members of the ENTHA subfamily[19,20].

Bottom Line: Our in silico analysis of this ENTH/ANTH/VHS superfamily, consisting of proteins gathered from 84 complete genomes representative of the different eukaryotic taxa, revealed that genomic distribution of this superfamily allows to discriminate Fungi and Metazoa from Plantae and Protists.Next, in a four way genome wide comparison, we showed that this discriminative feature is observed not only for other membrane trafficking effectors, but also for proteins involved in metabolism and in cytokinesis, suggesting that metabolism, cytokinesis and intracellular trafficking pathways co-evolved.Moreover, some of the proteins identified were implicated in multiple functions, in either trafficking and metabolism or trafficking and cytokinesis, suggesting that membrane trafficking is central to this co-evolution process.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Molecular and Cellular Genetics, UMR7156 CNRS/Université de Strasbourg, 21 rue Descartes, 67084, Strasbourg, France.

ABSTRACT

Background: Membrane trafficking involves the complex regulation of proteins and lipids intracellular localization and is required for metabolic uptake, cell growth and development. Different trafficking pathways passing through the endosomes are coordinated by the ENTH/ANTH/VHS adaptor protein superfamily. The endosomes are crucial for eukaryotes since the acquisition of the endomembrane system was a central process in eukaryogenesis.

Results: Our in silico analysis of this ENTH/ANTH/VHS superfamily, consisting of proteins gathered from 84 complete genomes representative of the different eukaryotic taxa, revealed that genomic distribution of this superfamily allows to discriminate Fungi and Metazoa from Plantae and Protists. Next, in a four way genome wide comparison, we showed that this discriminative feature is observed not only for other membrane trafficking effectors, but also for proteins involved in metabolism and in cytokinesis, suggesting that metabolism, cytokinesis and intracellular trafficking pathways co-evolved. Moreover, some of the proteins identified were implicated in multiple functions, in either trafficking and metabolism or trafficking and cytokinesis, suggesting that membrane trafficking is central to this co-evolution process.

Conclusions: Our study suggests that membrane trafficking and compartmentalization were not only key features for the emergence of eukaryotic cells but also drove the separation of the eukaryotes in the different taxa.

Show MeSH
Related in: MedlinePlus