Protein-protein interactions as determinants of operon architecture
Operons, clusters of genes under a single promoter, often exhibit a specific gene order influencing their physiological function. While functional relatedness is a known factor for clustering, the underlying drivers of gene ordering remain unclear. To investigate this, we analyzed the pdu operon, en...
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Published in | Biochimica et biophysica acta. General subjects Vol. 1869; no. 6; p. 130794 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
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Elsevier B.V
01.05.2025
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Abstract | Operons, clusters of genes under a single promoter, often exhibit a specific gene order influencing their physiological function. While functional relatedness is a known factor for clustering, the underlying drivers of gene ordering remain unclear. To investigate this, we analyzed the pdu operon, encoding proteins for 1,2 Pdu bacterial microcompartment. Our bioinformatics revealed no link between the sequence similarity and proximity of the genes in the operon. However quantitative mapping of protein-protein interactions within the operon using a barrage of spectroscopic tools showed a strong correlation between interaction strength and gene proximity. Our data thus indicates that protein-protein interactions play a significant role in determining gene order within the pdu operon, potentially contributing to the efficient assembly and function of these microcompartments.
[Display omitted]
•Gene order in the pdu operon is optimized for assembly, with adjacent genes showing stronger protein interactions.•Strong protein interactions form nanotubes, while weaker ones lead to less defined assemblies.•The study offers a framework for bioengineering, enabling synthetic bacterial microcompartments. |
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AbstractList | Operons, clusters of genes under a single promoter, often exhibit a specific gene order influencing their physiological function. While functional relatedness is a known factor for clustering, the underlying drivers of gene ordering remain unclear. To investigate this, we analyzed the pdu operon, encoding proteins for 1,2 Pdu bacterial microcompartment. Our bioinformatics revealed no link between the sequence similarity and proximity of the genes in the operon. However quantitative mapping of protein-protein interactions within the operon using a barrage of spectroscopic tools showed a strong correlation between interaction strength and gene proximity. Our data thus indicates that protein-protein interactions play a significant role in determining gene order within the pdu operon, potentially contributing to the efficient assembly and function of these microcompartments. Operons, clusters of genes under a single promoter, often exhibit a specific gene order influencing their physiological function. While functional relatedness is a known factor for clustering, the underlying drivers of gene ordering remain unclear. To investigate this, we analyzed the pdu operon, encoding proteins for 1,2 Pdu bacterial microcompartment. Our bioinformatics revealed no link between the sequence similarity and proximity of the genes in the operon. However quantitative mapping of protein-protein interactions within the operon using a barrage of spectroscopic tools showed a strong correlation between interaction strength and gene proximity. Our data thus indicates that protein-protein interactions play a significant role in determining gene order within the pdu operon, potentially contributing to the efficient assembly and function of these microcompartments.Operons, clusters of genes under a single promoter, often exhibit a specific gene order influencing their physiological function. While functional relatedness is a known factor for clustering, the underlying drivers of gene ordering remain unclear. To investigate this, we analyzed the pdu operon, encoding proteins for 1,2 Pdu bacterial microcompartment. Our bioinformatics revealed no link between the sequence similarity and proximity of the genes in the operon. However quantitative mapping of protein-protein interactions within the operon using a barrage of spectroscopic tools showed a strong correlation between interaction strength and gene proximity. Our data thus indicates that protein-protein interactions play a significant role in determining gene order within the pdu operon, potentially contributing to the efficient assembly and function of these microcompartments. Operons, clusters of genes under a single promoter, often exhibit a specific gene order influencing their physiological function. While functional relatedness is a known factor for clustering, the underlying drivers of gene ordering remain unclear. To investigate this, we analyzed the pdu operon, encoding proteins for 1,2 Pdu bacterial microcompartment. Our bioinformatics revealed no link between the sequence similarity and proximity of the genes in the operon. However quantitative mapping of protein-protein interactions within the operon using a barrage of spectroscopic tools showed a strong correlation between interaction strength and gene proximity. Our data thus indicates that protein-protein interactions play a significant role in determining gene order within the pdu operon, potentially contributing to the efficient assembly and function of these microcompartments. [Display omitted] •Gene order in the pdu operon is optimized for assembly, with adjacent genes showing stronger protein interactions.•Strong protein interactions form nanotubes, while weaker ones lead to less defined assemblies.•The study offers a framework for bioengineering, enabling synthetic bacterial microcompartments. |
ArticleNumber | 130794 |
Author | Negi, Preeti Rose, S.M. Bedi, Silky Sinha, Sharmistha Kaur, Simerpreet |
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Cites_doi | 10.1128/JB.00785-16 10.1093/nar/gkae241 10.1016/j.saa.2012.02.088 10.1016/j.molcel.2010.04.008 10.1038/s41467-022-31279-3 10.1016/j.celrep.2015.12.085 10.1021/bi00745a020 10.1073/pnas.1207516109 10.1016/S0022-2836(61)80072-7 10.1039/C8RA00210J 10.1371/journal.pcbi.1004067 10.1126/science.aan3289 10.1371/journal.pcbi.1011038 10.1016/j.jmb.2020.11.020 10.1128/jb.00576-21 10.1039/D3TB00098B 10.1021/bi980274n 10.1128/JB.01473-10 10.3390/metabo5020252 10.1038/nrmicro787 10.1042/BST20170564 |
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Keywords | Operonic arrangement Self-assembly FRET Protein-protein interactions |
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Bacteriol. doi: 10.1128/JB.01473-10 – volume: 14 year: 2018 ident: 10.1016/j.bbagen.2025.130794_bb0080 article-title: A generic self-assembly process in microcompartments and synthetic protein nanotubes publication-title: Small – volume: 5 start-page: 252 year: 2015 ident: 10.1016/j.bbagen.2025.130794_bb0115 article-title: Footprints of optimal protein assembly strategies in the operonic structure of prokaryotes publication-title: Metabolites doi: 10.3390/metabo5020252 – volume: 2 start-page: 57 year: 2004 ident: 10.1016/j.bbagen.2025.130794_bb0010 article-title: The regulation of bacterial transcription initiation publication-title: Nat. Rev. Microbiol. doi: 10.1038/nrmicro787 – volume: 29 start-page: 1727 year: 1960 ident: 10.1016/j.bbagen.2025.130794_bb0005 article-title: The operon: a group of genes whose expression is coordinated by an operator publication-title: J. 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SubjectTerms | Bacterial Proteins - genetics Bacterial Proteins - metabolism Computational Biology - methods Escherichia coli - genetics Escherichia coli - metabolism FRET Operon - genetics Operonic arrangement Protein Interaction Mapping Protein Interaction Maps Protein-protein interactions Self-assembly |
Title | Protein-protein interactions as determinants of operon architecture |
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