The Repertoire of Solute-Binding Proteins of Model Bacteria Reveals Large Differences in Number, Type, and Ligand Range
ABSTRACT Solute-binding proteins (SBPs) are of central physiological relevance for bacteria. They are located in the extracytosolic space, where they present substrates to transporters but also stimulate different types of transmembrane receptors coordinating compound uptake with signal transduction...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-10-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02054-22 |
| _version_ | 1811257713630380032 |
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| author | Álvaro Ortega Miguel A. Matilla Tino Krell |
| author_facet | Álvaro Ortega Miguel A. Matilla Tino Krell |
| author_sort | Álvaro Ortega |
| collection | DOAJ |
| description | ABSTRACT Solute-binding proteins (SBPs) are of central physiological relevance for bacteria. They are located in the extracytosolic space, where they present substrates to transporters but also stimulate different types of transmembrane receptors coordinating compound uptake with signal transduction. SBPs are a superfamily composed of proteins recognized by 45 Pfam profiles. The definition of SBP profiles for bacteria is hampered by the fact that these Pfam profiles recognize sensor domains for different types of signaling proteins or cytosolic proteins with alternative functions. We report here the retrieval of the SBPs from 49 bacterial model strains with different lifestyles and phylogenetic distributions. Proteins were manually curated, and the ligands recognized were predicted bioinformatically. There were very large differences in the number and type of SBPs between strains, ranging from 7 SBPs in Helicobacter pylori 26695 to 189 SBPs in Sinorhizobium meliloti 1021. SBPs were found to represent 0.22 to 5.13% of the total protein-encoding genes. The abundance of SBPs was largely determined by strain phylogeny, and no obvious link with the bacterial lifestyle was noted. Most abundant (36%) were SBPs predicted to recognize amino acids or peptides, followed by those expected to bind different sugars (18%). To the best of our knowledge, this is the first comparative study of bacterial SBP repertoires. Given the importance of SBPs in nutrient uptake and signaling, this study enhances the knowledge of model bacteria and will permit the definition of SBP profiles of other strains. IMPORTANCE SBPs are essential components for many transporters, but multiple pieces of more recent evidence indicate that the SBP-mediated stimulation of different transmembrane receptors is a general and widespread signal transduction mechanism in bacteria. The double function of SBPs in coordinating transport with signal transduction remains to a large degree unexplored and represents a major research need. The definition of the SBP repertoire of the 49 bacterial model strains examined here, along with information on their cognate ligand profiles forms the basis to close this gap in knowledge. Furthermore, this study provides information on the forces that have driven the evolution of transporters with different ligand specificities in bacteria that differ in phylogenetics and lifestyle. This article is also a first step in setting up automatic algorithms that permit the large-scale identification of the SBP repertoire in proteomes. |
| first_indexed | 2024-04-12T18:01:45Z |
| format | Article |
| id | doaj.art-c3b365cf121b4f02b713971c679a8b93 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-12T18:01:45Z |
| publishDate | 2022-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-c3b365cf121b4f02b713971c679a8b932022-12-22T03:22:09ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-10-0110510.1128/spectrum.02054-22The Repertoire of Solute-Binding Proteins of Model Bacteria Reveals Large Differences in Number, Type, and Ligand RangeÁlvaro Ortega0Miguel A. Matilla1Tino Krell2Department of Biochemistry and Molecular Biology B and Immunology, Faculty of Chemistry, University of Murcia, Regional Campus of International Excellence Campus Mare Nostrum, Murcia, SpainDepartment of Environmental Protection, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainDepartment of Environmental Protection, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainABSTRACT Solute-binding proteins (SBPs) are of central physiological relevance for bacteria. They are located in the extracytosolic space, where they present substrates to transporters but also stimulate different types of transmembrane receptors coordinating compound uptake with signal transduction. SBPs are a superfamily composed of proteins recognized by 45 Pfam profiles. The definition of SBP profiles for bacteria is hampered by the fact that these Pfam profiles recognize sensor domains for different types of signaling proteins or cytosolic proteins with alternative functions. We report here the retrieval of the SBPs from 49 bacterial model strains with different lifestyles and phylogenetic distributions. Proteins were manually curated, and the ligands recognized were predicted bioinformatically. There were very large differences in the number and type of SBPs between strains, ranging from 7 SBPs in Helicobacter pylori 26695 to 189 SBPs in Sinorhizobium meliloti 1021. SBPs were found to represent 0.22 to 5.13% of the total protein-encoding genes. The abundance of SBPs was largely determined by strain phylogeny, and no obvious link with the bacterial lifestyle was noted. Most abundant (36%) were SBPs predicted to recognize amino acids or peptides, followed by those expected to bind different sugars (18%). To the best of our knowledge, this is the first comparative study of bacterial SBP repertoires. Given the importance of SBPs in nutrient uptake and signaling, this study enhances the knowledge of model bacteria and will permit the definition of SBP profiles of other strains. IMPORTANCE SBPs are essential components for many transporters, but multiple pieces of more recent evidence indicate that the SBP-mediated stimulation of different transmembrane receptors is a general and widespread signal transduction mechanism in bacteria. The double function of SBPs in coordinating transport with signal transduction remains to a large degree unexplored and represents a major research need. The definition of the SBP repertoire of the 49 bacterial model strains examined here, along with information on their cognate ligand profiles forms the basis to close this gap in knowledge. Furthermore, this study provides information on the forces that have driven the evolution of transporters with different ligand specificities in bacteria that differ in phylogenetics and lifestyle. This article is also a first step in setting up automatic algorithms that permit the large-scale identification of the SBP repertoire in proteomes.https://journals.asm.org/doi/10.1128/spectrum.02054-22solute-binding proteinstransportsignal transductionmodel bacteriatransport substratesignal molecules |
| spellingShingle | Álvaro Ortega Miguel A. Matilla Tino Krell The Repertoire of Solute-Binding Proteins of Model Bacteria Reveals Large Differences in Number, Type, and Ligand Range Microbiology Spectrum solute-binding proteins transport signal transduction model bacteria transport substrate signal molecules |
| title | The Repertoire of Solute-Binding Proteins of Model Bacteria Reveals Large Differences in Number, Type, and Ligand Range |
| title_full | The Repertoire of Solute-Binding Proteins of Model Bacteria Reveals Large Differences in Number, Type, and Ligand Range |
| title_fullStr | The Repertoire of Solute-Binding Proteins of Model Bacteria Reveals Large Differences in Number, Type, and Ligand Range |
| title_full_unstemmed | The Repertoire of Solute-Binding Proteins of Model Bacteria Reveals Large Differences in Number, Type, and Ligand Range |
| title_short | The Repertoire of Solute-Binding Proteins of Model Bacteria Reveals Large Differences in Number, Type, and Ligand Range |
| title_sort | repertoire of solute binding proteins of model bacteria reveals large differences in number type and ligand range |
| topic | solute-binding proteins transport signal transduction model bacteria transport substrate signal molecules |
| url | https://journals.asm.org/doi/10.1128/spectrum.02054-22 |
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