Mechanism of NanR gene repression and allosteric induction of bacterial sialic acid metabolism

  • Christopher R. Horne
  • , Hariprasad Venugopal
  • , Santosh Panjikar
  • , David M. Wood
  • , Amy Henrickson
  • , Emre Brookes
  • , Rachel A. North
  • , James M. Murphy
  • , Rosmarie Friemann
  • , Michael D.W. Griffin
  • , Georg Ramm
  • , Borries Demeler
  • , Renwick C.J. Dobson

Research output: Contribution to journalArticlepeer-review

27 Scopus citations

Abstract

Bacteria respond to environmental changes by inducing transcription of some genes and repressing others. Sialic acids, which coat human cell surfaces, are a nutrient source for pathogenic and commensal bacteria. The Escherichia coli GntR-type transcriptional repressor, NanR, regulates sialic acid metabolism, but the mechanism is unclear. Here, we demonstrate that three NanR dimers bind a (GGTATA)3-repeat operator cooperatively and with high affinity. Single-particle cryo-electron microscopy structures reveal the DNA-binding domain is reorganized to engage DNA, while three dimers assemble in close proximity across the (GGTATA)3-repeat operator. Such an interaction allows cooperative protein-protein interactions between NanR dimers via their N-terminal extensions. The effector, N-acetylneuraminate, binds NanR and attenuates the NanR-DNA interaction. The crystal structure of NanR in complex with N-acetylneuraminate reveals a domain rearrangement upon N-acetylneuraminate binding to lock NanR in a conformation that weakens DNA binding. Our data provide a molecular basis for the regulation of bacterial sialic acid metabolism.

Original languageEnglish
Article number1988
JournalNature Communications
Volume12
Issue number1
DOIs
StatePublished - Dec 1 2021

Funding

We thank staff at the Australian Synchrotron MX2 and SAXS/WAXS beamlines for their assistance in data collection and the New Zealand Synchrotron Group for enabling access; Janet Newman (Collaborative Crystallisation Centre) for assistance with protein crystallization, Yee-Foong Mok (Bio21 Institute, University of Melbourne) for his assistance with analytical ultracentrifugation experiments; and Tim Cooper (Massey University) for critical reading of the manuscript. We are grateful to the Biomolecular Interaction Centre (University of Canterbury), the Canterbury Medical Research Foundation, and the Maurice Wilkins Centre for scholarship support to C.R.H. We acknowledge the New Zealand Royal Society Marsden Fund (to R.C.J.D., UOC1506), Ministry of Business, Innovation and Employment Smart Ideas grant (to R.C.J.D., UOCX1706), ARC LIEF grants (to G.R., LE120100090 and LE200100045), Swedish Governmental Agency for Innovation Systems (to R.F., 2017-00180), Centre for Antibiotic Resistance Research (CARe) at University of Gothenburg (to R.F.), NHMRC grants (to J.M.M., 1172929 and 9000653), and the Victorian Government Operational Infrastructure Support Scheme (to J.M.M.). Funding to B.D. from NIH for grant and UltraScan multiwavelength development support (GM120600 and NSF-ACI-1339649), NSF/XSEDE grant for support towards UltraScan supercomputer calculations (TG-MCB070039N), and University of Texas grant (TG457201) is acknowledged. This research was undertaken in part using the SAXS/WAXS and MX2 beamlines at the Australian Synchrotron, part of ANSTO, and made use of the ACRF detector; the Monash Ramaciotti Centre for Cryo-Electron Microscopy (a node of Microscopy Australia) and made use of the Multi-modal Australian ScienceS Imaging and Visualisation Environment (www.massive.org.au) for data processing; and the Canadian Center for Hydrodynamics, University of Lethbridge for MWL-SV experiments, with support from the Canada Foundation for Innovation Grant CFI-37589 (to B.D.).

FundersFunder number
TG457201
TG-MCB070039N
NSF-ACI-1339649
R01GM120600
University of Canterbury
Canada Foundation for InnovationCFI-37589
Australian Research CouncilLE200100045, LE120100090
1172929, 9000653
UOC1506
2017-00180
Ministry of Business, Innovation and EmploymentUOCX1706
State Government of Victoria

    Fingerprint

    Dive into the research topics of 'Mechanism of NanR gene repression and allosteric induction of bacterial sialic acid metabolism'. Together they form a unique fingerprint.

    Cite this