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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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Related in: MedlinePlus

Genomic distribution of the ENTH/ANTH/VHS superfamily members. The presence or absence of all superfamily members was established by BLASTP searches. The number of rectangles in a subfamily of a given organism corresponds to the number of protein types in this subfamily. The number in a given type corresponds to the number of indistinguishable subtypes. Organism disposition is based on the phylogeny proposed by Cavalier-Smith (Cavalier-Smith 2010).
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Figure 2: Genomic distribution of the ENTH/ANTH/VHS superfamily members. The presence or absence of all superfamily members was established by BLASTP searches. The number of rectangles in a subfamily of a given organism corresponds to the number of protein types in this subfamily. The number in a given type corresponds to the number of indistinguishable subtypes. Organism disposition is based on the phylogeny proposed by Cavalier-Smith (Cavalier-Smith 2010).

Mentions: After validating our clustering, we assessed the genomic distribution of the ENTH/ANTH/VHS members in the analyzed species (Figure2). The presence/absence profile recapitulates the proposed evolution of the endocytic system[17] with Metazoa and Fungi (Opisthokonta supergroup) being closer to the Amoebozoa than to Plantae, Chromista, Excavata, Rhizaria and Euglenozoa subfamilies. Opisthokonta possess the most complex panel with protein members in at least eight of the ten different subfamilies while Amoebozoa display four distinct subfamilies with the presence of ANTH-containing proteins (otherwise Opisthokonta-specific proteins) in the two studied organisms D. discoideum and E. histolitica. Plantae and Euglenozoa have representatives only in ENTHA, PICALM and GGA subfamilies while Chromista and Excavata only in the ENTHA subfamily (Figure2). This suggests that the ENTHA, PICALM and GGA subfamilies conserved in different taxa were present prior to the formation of the different eukaryotic supergroups.


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)

Genomic distribution of the ENTH/ANTH/VHS superfamily members. The presence or absence of all superfamily members was established by BLASTP searches. The number of rectangles in a subfamily of a given organism corresponds to the number of protein types in this subfamily. The number in a given type corresponds to the number of indistinguishable subtypes. Organism disposition is based on the phylogeny proposed by Cavalier-Smith (Cavalier-Smith 2010).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Genomic distribution of the ENTH/ANTH/VHS superfamily members. The presence or absence of all superfamily members was established by BLASTP searches. The number of rectangles in a subfamily of a given organism corresponds to the number of protein types in this subfamily. The number in a given type corresponds to the number of indistinguishable subtypes. Organism disposition is based on the phylogeny proposed by Cavalier-Smith (Cavalier-Smith 2010).
Mentions: After validating our clustering, we assessed the genomic distribution of the ENTH/ANTH/VHS members in the analyzed species (Figure2). The presence/absence profile recapitulates the proposed evolution of the endocytic system[17] with Metazoa and Fungi (Opisthokonta supergroup) being closer to the Amoebozoa than to Plantae, Chromista, Excavata, Rhizaria and Euglenozoa subfamilies. Opisthokonta possess the most complex panel with protein members in at least eight of the ten different subfamilies while Amoebozoa display four distinct subfamilies with the presence of ANTH-containing proteins (otherwise Opisthokonta-specific proteins) in the two studied organisms D. discoideum and E. histolitica. Plantae and Euglenozoa have representatives only in ENTHA, PICALM and GGA subfamilies while Chromista and Excavata only in the ENTHA subfamily (Figure2). This suggests that the ENTHA, PICALM and GGA subfamilies conserved in different taxa were present prior to the formation of the different eukaryotic supergroups.

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