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Distribution, classification, domain architectures and evolution of prolyl oligopeptidases in prokaryotic lineages.

Kaushik S, Sowdhamini R - BMC Genomics (2014)

Bottom Line: We proposed significant extension of this gene family by characterizing 39 new POPs and 158 new α/β hydrolase members.Many genomes with multiple POPs were identified with high sequence variations and different cellular localizations.Such anomalous distribution of POP genes in different bacterial genomes shows differential expansion of POP gene family primarily by multiple horizontal gene transfer events.

View Article: PubMed Central - PubMed

Affiliation: National Centre for Biological Sciences, Tata Institute of Fundamental Research, GKVK Campus, Bellary Road, Bangalore, 560065, India. Swati.Kaushik@ucsf.edu.

ABSTRACT

Background: Prolyl oligopeptidases (POPs) are proteolytic enzymes, widely distributed in all the kingdoms of life. Bacterial POPs are pharmaceutically important enzymes, yet their functional and evolutionary details are not fully explored. Therefore, current analysis is aimed at understanding the distribution, domain architecture, probable biological functions and gene family expansion of POPs in bacterial and archaeal lineages.

Results: Exhaustive sequence analysis of 1,202 bacterial and 91 archaeal genomes revealed ~3,000 POP homologs, with only 638 annotated POPs. We observed wide distribution of POPs in all the analysed bacterial lineages. Phylogenetic analysis and co-clustering of POPs of different phyla suggested their common functions in all the prokaryotic species. Further, on the basis of unique sequence motifs we could classify bacterial POPs into eight subtypes. Analysis of coexisting domains in POPs highlighted their involvement in protein-protein interactions and cellular signaling. We proposed significant extension of this gene family by characterizing 39 new POPs and 158 new α/β hydrolase members.

Conclusions: Our study reflects diversity and functional importance of POPs in bacterial species. Many genomes with multiple POPs were identified with high sequence variations and different cellular localizations. Such anomalous distribution of POP genes in different bacterial genomes shows differential expansion of POP gene family primarily by multiple horizontal gene transfer events.

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Related in: MedlinePlus

Phylogenetic analysis of annotated bPOPs. Color code: Thermotogae-cyan, Firmicutes-lime, Chloroflexi-green, Deinococcus-thermus-blue, Chlorobi-magenta, Actinobacteria-blue, Acidobacteria-yellow, Alphaproteobacteria-teal, Betaproteobacteria-grey, Gammaproteobacteria-olive, Deltaproteobacteria-blue, Bacteriodetes-black, Planctomycetes-black, Cyanobacteria-purple, Gemmatimonadetes-Red branch with species name in black, Spirochaetes-pink branch with species name in black, Fibrobacteres-light grey, Archaebacteria-red. Nine distinct clusters are marked in red.
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Fig6: Phylogenetic analysis of annotated bPOPs. Color code: Thermotogae-cyan, Firmicutes-lime, Chloroflexi-green, Deinococcus-thermus-blue, Chlorobi-magenta, Actinobacteria-blue, Acidobacteria-yellow, Alphaproteobacteria-teal, Betaproteobacteria-grey, Gammaproteobacteria-olive, Deltaproteobacteria-blue, Bacteriodetes-black, Planctomycetes-black, Cyanobacteria-purple, Gemmatimonadetes-Red branch with species name in black, Spirochaetes-pink branch with species name in black, Fibrobacteres-light grey, Archaebacteria-red. Nine distinct clusters are marked in red.

Mentions: To investigate the differences in the annotated bPOPs, we next performed phylogenetic clustering of 638 annotated POPs that showed nine distinct clusters, with co-clustering among members of different phyla (Figure 6). This co-clustering trend and absence of phylum-specific clusters suggested high conservation of POPs within bacterial lineages. Genus Shewanella of marine metal-reducing bacteria was highly populated with considerable number of annotated bPOPs in all the nine clusters. Similarly, archaeal POPs were also co-clustered well with other bPOPs. This co-clustering suggested the possibility of lateral transfer of POP genes among bacteria and between archaeal and bacterial species (Additional files 4 and 8).Figure 6


Distribution, classification, domain architectures and evolution of prolyl oligopeptidases in prokaryotic lineages.

Kaushik S, Sowdhamini R - BMC Genomics (2014)

Phylogenetic analysis of annotated bPOPs. Color code: Thermotogae-cyan, Firmicutes-lime, Chloroflexi-green, Deinococcus-thermus-blue, Chlorobi-magenta, Actinobacteria-blue, Acidobacteria-yellow, Alphaproteobacteria-teal, Betaproteobacteria-grey, Gammaproteobacteria-olive, Deltaproteobacteria-blue, Bacteriodetes-black, Planctomycetes-black, Cyanobacteria-purple, Gemmatimonadetes-Red branch with species name in black, Spirochaetes-pink branch with species name in black, Fibrobacteres-light grey, Archaebacteria-red. Nine distinct clusters are marked in red.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4522959&req=5

Fig6: Phylogenetic analysis of annotated bPOPs. Color code: Thermotogae-cyan, Firmicutes-lime, Chloroflexi-green, Deinococcus-thermus-blue, Chlorobi-magenta, Actinobacteria-blue, Acidobacteria-yellow, Alphaproteobacteria-teal, Betaproteobacteria-grey, Gammaproteobacteria-olive, Deltaproteobacteria-blue, Bacteriodetes-black, Planctomycetes-black, Cyanobacteria-purple, Gemmatimonadetes-Red branch with species name in black, Spirochaetes-pink branch with species name in black, Fibrobacteres-light grey, Archaebacteria-red. Nine distinct clusters are marked in red.
Mentions: To investigate the differences in the annotated bPOPs, we next performed phylogenetic clustering of 638 annotated POPs that showed nine distinct clusters, with co-clustering among members of different phyla (Figure 6). This co-clustering trend and absence of phylum-specific clusters suggested high conservation of POPs within bacterial lineages. Genus Shewanella of marine metal-reducing bacteria was highly populated with considerable number of annotated bPOPs in all the nine clusters. Similarly, archaeal POPs were also co-clustered well with other bPOPs. This co-clustering suggested the possibility of lateral transfer of POP genes among bacteria and between archaeal and bacterial species (Additional files 4 and 8).Figure 6

Bottom Line: We proposed significant extension of this gene family by characterizing 39 new POPs and 158 new α/β hydrolase members.Many genomes with multiple POPs were identified with high sequence variations and different cellular localizations.Such anomalous distribution of POP genes in different bacterial genomes shows differential expansion of POP gene family primarily by multiple horizontal gene transfer events.

View Article: PubMed Central - PubMed

Affiliation: National Centre for Biological Sciences, Tata Institute of Fundamental Research, GKVK Campus, Bellary Road, Bangalore, 560065, India. Swati.Kaushik@ucsf.edu.

ABSTRACT

Background: Prolyl oligopeptidases (POPs) are proteolytic enzymes, widely distributed in all the kingdoms of life. Bacterial POPs are pharmaceutically important enzymes, yet their functional and evolutionary details are not fully explored. Therefore, current analysis is aimed at understanding the distribution, domain architecture, probable biological functions and gene family expansion of POPs in bacterial and archaeal lineages.

Results: Exhaustive sequence analysis of 1,202 bacterial and 91 archaeal genomes revealed ~3,000 POP homologs, with only 638 annotated POPs. We observed wide distribution of POPs in all the analysed bacterial lineages. Phylogenetic analysis and co-clustering of POPs of different phyla suggested their common functions in all the prokaryotic species. Further, on the basis of unique sequence motifs we could classify bacterial POPs into eight subtypes. Analysis of coexisting domains in POPs highlighted their involvement in protein-protein interactions and cellular signaling. We proposed significant extension of this gene family by characterizing 39 new POPs and 158 new α/β hydrolase members.

Conclusions: Our study reflects diversity and functional importance of POPs in bacterial species. Many genomes with multiple POPs were identified with high sequence variations and different cellular localizations. Such anomalous distribution of POP genes in different bacterial genomes shows differential expansion of POP gene family primarily by multiple horizontal gene transfer events.

Show MeSH
Related in: MedlinePlus