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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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Sequence variations of the POPs of multi-POP bacterial genomes. Numbers of putative POPs identified in these genomes are shown in brackets.
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Fig9: Sequence variations of the POPs of multi-POP bacterial genomes. Numbers of putative POPs identified in these genomes are shown in brackets.

Mentions: While performing the sequence analysis, we noticed high variations in the number of annotated POP genes in bacterial genomes, ranging from no POPs to multiple copies of POPs within a genome. Overall, out of 269 identified bacterial genomes with annotated POPs, 148 had a single copy of POP gene. The overrepresentation of POP was particularly observed in genus Shewanella of Gammaproteobacteria, where most of the species had multiple copies of POP gene. One of the interesting examples of multi-POP proteome was Shewanella woodyi with 16 POPs sharing an average sequence identity of 15% (ranging from 8 to 35%). Moreover, we could identify 12 copies of POP gene in Shewanella piezotolerans, and 10 copies each in Shewanella pealeana and Shewanella sediminis. Besides genus Shewanella, 15 POP genes were also identified in Solibacter usitatus. High sequence variations in paralogs of POP suggested that they are not closely related to each other, except in S. thermophilus genome (Figure 9, Additional file 4). These multiple POPs within a genome also differ in their cellular localizations (Additional file 1-S1a).Figure 9


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

Kaushik S, Sowdhamini R - BMC Genomics (2014)

Sequence variations of the POPs of multi-POP bacterial genomes. Numbers of putative POPs identified in these genomes are shown in brackets.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig9: Sequence variations of the POPs of multi-POP bacterial genomes. Numbers of putative POPs identified in these genomes are shown in brackets.
Mentions: While performing the sequence analysis, we noticed high variations in the number of annotated POP genes in bacterial genomes, ranging from no POPs to multiple copies of POPs within a genome. Overall, out of 269 identified bacterial genomes with annotated POPs, 148 had a single copy of POP gene. The overrepresentation of POP was particularly observed in genus Shewanella of Gammaproteobacteria, where most of the species had multiple copies of POP gene. One of the interesting examples of multi-POP proteome was Shewanella woodyi with 16 POPs sharing an average sequence identity of 15% (ranging from 8 to 35%). Moreover, we could identify 12 copies of POP gene in Shewanella piezotolerans, and 10 copies each in Shewanella pealeana and Shewanella sediminis. Besides genus Shewanella, 15 POP genes were also identified in Solibacter usitatus. High sequence variations in paralogs of POP suggested that they are not closely related to each other, except in S. thermophilus genome (Figure 9, Additional file 4). These multiple POPs within a genome also differ in their cellular localizations (Additional file 1-S1a).Figure 9

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