A new class of binding-protein dependent solute transporter exemplified by the TAXI-GltS system from Bordetella pertussis
Abstract Tripartite ATP-independent periplasmic (TRAP) transporters are widespread in prokaryotes, but absent in eukaryotes, and transport various substrates. TRAP transporters are typically composed of a monomeric substrate binding protein (SBP) and a characteristic transmembrane component. Here, w...
Saved in:
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2025-08-01
|
| Series: | Communications Biology |
| Online Access: | https://doi.org/10.1038/s42003-025-08591-x |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1849235018198548480 |
|---|---|
| author | Lily M. Jaques Joseph F. S. Davies Jack J. Sheldon-Towler David J. Kelly Vanessa Leone Christopher Mulligan |
| author_facet | Lily M. Jaques Joseph F. S. Davies Jack J. Sheldon-Towler David J. Kelly Vanessa Leone Christopher Mulligan |
| author_sort | Lily M. Jaques |
| collection | DOAJ |
| description | Abstract Tripartite ATP-independent periplasmic (TRAP) transporters are widespread in prokaryotes, but absent in eukaryotes, and transport various substrates. TRAP transporters are typically composed of a monomeric substrate binding protein (SBP) and a characteristic transmembrane component. Here, we describe the discovery and characterisation of a TRAP SBP from the TAXI subfamily with a previously unidentified architecture. BP0403 from Bordetella pertussis is a predicted lipoprotein with 3 distinct domains; an α/β globular domain, a helical domain and a C-terminal TAXI SBP domain. Characterisation of full-length BP0403 reveals that it forms a stable dimer, and structural modelling coupled with molecular weight analysis reveals that the interdomain helical region is solely responsible for dimerisation. Differential scanning fluorimetry (DSF) and intrinsic tyrosine fluorescence reveal that BP0403 binds L-glutamate with nanomolar affinity. Unexpectedly, genome context analysis of BP0403 reveals no TRAP membrane component genes; instead, we find co-localisation and translational coupling with gltS, encoding a Na+/glutamate symporter. In other bacteria, we identified fused BP0403-GltS homologues, strongly suggesting that this constitutes a completely novel SBP-dependent secondary active transporter. Structural comparisons suggest GltS operates by an elevator-type mechanism, like TRAP transporters; the association of an SBP with this class of secondary transporter is an emerging theme. |
| format | Article |
| id | doaj-art-7db72f4e03004aed918c7ef9b701e9f0 |
| institution | Kabale University |
| issn | 2399-3642 |
| language | English |
| publishDate | 2025-08-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Communications Biology |
| spelling | doaj-art-7db72f4e03004aed918c7ef9b701e9f02025-08-20T04:02:56ZengNature PortfolioCommunications Biology2399-36422025-08-018111110.1038/s42003-025-08591-xA new class of binding-protein dependent solute transporter exemplified by the TAXI-GltS system from Bordetella pertussisLily M. Jaques0Joseph F. S. Davies1Jack J. Sheldon-Towler2David J. Kelly3Vanessa Leone4Christopher Mulligan5School of Biosciences, Division of Natural Sciences, University of KentSchool of Biosciences, Division of Natural Sciences, University of KentSchool of Biosciences, Division of Natural Sciences, University of KentSchool of Biosciences, The University of SheffieldDepartment of Biophysics and Data Science Institute, Medical College of WisconsinSchool of Biosciences, Division of Natural Sciences, University of KentAbstract Tripartite ATP-independent periplasmic (TRAP) transporters are widespread in prokaryotes, but absent in eukaryotes, and transport various substrates. TRAP transporters are typically composed of a monomeric substrate binding protein (SBP) and a characteristic transmembrane component. Here, we describe the discovery and characterisation of a TRAP SBP from the TAXI subfamily with a previously unidentified architecture. BP0403 from Bordetella pertussis is a predicted lipoprotein with 3 distinct domains; an α/β globular domain, a helical domain and a C-terminal TAXI SBP domain. Characterisation of full-length BP0403 reveals that it forms a stable dimer, and structural modelling coupled with molecular weight analysis reveals that the interdomain helical region is solely responsible for dimerisation. Differential scanning fluorimetry (DSF) and intrinsic tyrosine fluorescence reveal that BP0403 binds L-glutamate with nanomolar affinity. Unexpectedly, genome context analysis of BP0403 reveals no TRAP membrane component genes; instead, we find co-localisation and translational coupling with gltS, encoding a Na+/glutamate symporter. In other bacteria, we identified fused BP0403-GltS homologues, strongly suggesting that this constitutes a completely novel SBP-dependent secondary active transporter. Structural comparisons suggest GltS operates by an elevator-type mechanism, like TRAP transporters; the association of an SBP with this class of secondary transporter is an emerging theme.https://doi.org/10.1038/s42003-025-08591-x |
| spellingShingle | Lily M. Jaques Joseph F. S. Davies Jack J. Sheldon-Towler David J. Kelly Vanessa Leone Christopher Mulligan A new class of binding-protein dependent solute transporter exemplified by the TAXI-GltS system from Bordetella pertussis Communications Biology |
| title | A new class of binding-protein dependent solute transporter exemplified by the TAXI-GltS system from Bordetella pertussis |
| title_full | A new class of binding-protein dependent solute transporter exemplified by the TAXI-GltS system from Bordetella pertussis |
| title_fullStr | A new class of binding-protein dependent solute transporter exemplified by the TAXI-GltS system from Bordetella pertussis |
| title_full_unstemmed | A new class of binding-protein dependent solute transporter exemplified by the TAXI-GltS system from Bordetella pertussis |
| title_short | A new class of binding-protein dependent solute transporter exemplified by the TAXI-GltS system from Bordetella pertussis |
| title_sort | new class of binding protein dependent solute transporter exemplified by the taxi glts system from bordetella pertussis |
| url | https://doi.org/10.1038/s42003-025-08591-x |
| work_keys_str_mv | AT lilymjaques anewclassofbindingproteindependentsolutetransporterexemplifiedbythetaxigltssystemfrombordetellapertussis AT josephfsdavies anewclassofbindingproteindependentsolutetransporterexemplifiedbythetaxigltssystemfrombordetellapertussis AT jackjsheldontowler anewclassofbindingproteindependentsolutetransporterexemplifiedbythetaxigltssystemfrombordetellapertussis AT davidjkelly anewclassofbindingproteindependentsolutetransporterexemplifiedbythetaxigltssystemfrombordetellapertussis AT vanessaleone anewclassofbindingproteindependentsolutetransporterexemplifiedbythetaxigltssystemfrombordetellapertussis AT christophermulligan anewclassofbindingproteindependentsolutetransporterexemplifiedbythetaxigltssystemfrombordetellapertussis AT lilymjaques newclassofbindingproteindependentsolutetransporterexemplifiedbythetaxigltssystemfrombordetellapertussis AT josephfsdavies newclassofbindingproteindependentsolutetransporterexemplifiedbythetaxigltssystemfrombordetellapertussis AT jackjsheldontowler newclassofbindingproteindependentsolutetransporterexemplifiedbythetaxigltssystemfrombordetellapertussis AT davidjkelly newclassofbindingproteindependentsolutetransporterexemplifiedbythetaxigltssystemfrombordetellapertussis AT vanessaleone newclassofbindingproteindependentsolutetransporterexemplifiedbythetaxigltssystemfrombordetellapertussis AT christophermulligan newclassofbindingproteindependentsolutetransporterexemplifiedbythetaxigltssystemfrombordetellapertussis |