A single intact ATPase site of the ABC transporter BtuCD drives 5% transport activity yet supports full in vivo vitamin B12 utilization

Proc Natl Acad Sci U S A. 2013 Apr 2;110(14):5434-9. doi: 10.1073/pnas.1209644110. Epub 2013 Mar 19.

Abstract

In all kingdoms of life, ATP binding cassette (ABC) transporters are essential to many cellular functions. In this large superfamily of proteins, two catalytic sites hydrolyze ATP to power uphill substrate translocation. A central question in the field concerns the relationship between the two ATPase catalytic sites: Are the sites independent of one another? Are both needed for function? Do they function cooperatively? These issues have been resolved for type I ABC transporters but never for a type II ABC transporter. The many mechanistic differences between type I and type II ABC transporters raise the question whether in respect to ATP hydrolysis the two subtypes are similar or different. We have addressed this question by studying the Escherichia coli vitamin B12 type II ABC transporter BtuCD. We have constructed and purified a series of BtuCD variants where both, one, or none of the ATPase sites were rendered inactive by mutation. We find that, in a membrane environment, the ATPase sites of BtuCD are highly cooperative with a Hill coefficient of 2. We also find that, when one of the ATPase sites is inactive, ATP hydrolysis and vitamin B12 transport by BtuCD is reduced by 95%. These exact features are also shared by the archetypical type I maltose ABC transporter. Remarkably, mutants that have lost 95% of their ATPase and transport capabilities still retain the ability to fully use vitamin B12 in vivo. The results demonstrate that, despite the many differences between type I and type II ABC transporters, the fundamental mechanism of ATP hydrolysis remains conserved.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP-Binding Cassette Transporters / genetics
  • ATP-Binding Cassette Transporters / metabolism*
  • Adenosine Triphosphatases / metabolism*
  • Adenosine Triphosphate / metabolism*
  • Biological Transport, Active / genetics
  • Biological Transport, Active / physiology
  • Catalytic Domain / genetics
  • Chromatography, Gel
  • Escherichia coli
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism*
  • Hydrolysis
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / metabolism*
  • Mutation / genetics
  • Vitamin B 12 / metabolism

Substances

  • ATP-Binding Cassette Transporters
  • BtuC peptide, E coli
  • BtuD peptide, E coli
  • Escherichia coli Proteins
  • Multiprotein Complexes
  • Adenosine Triphosphate
  • Adenosine Triphosphatases
  • Vitamin B 12