Comparative genomics and functional analysis of the NiaP family uncover nicotinate transporters from bacteria, plants, and mammals

Linda Jeanguenin, Aurora Lara-Núñez, Dmitry A. Rodionov, Andrei L. Osterman, Nataliya Y. Komarova, Doris Rentsch, Jesse F. Gregory, Andrew D. Hanson

Research output: Contribution to journalArticlepeer-review

21 Scopus citations

Abstract

The transporter(s) that mediate uptake of nicotinate and its N-methyl derivative trigonelline are not known in plants, and certain mammalian nicotinate transporters also remain unidentified. Potential candidates for these missing transporters include proteins from the ubiquitous NiaP family. In bacteria, niaP genes often belong to NAD-related regulons, and genetic evidence supports a role for Bacillus subtilis and Acinetobacter baumannii NiaP proteins in uptake of nicotinate or nicotinamide. Other bacterial niaP genes are, however, not in NAD-related regulons but cluster on the chromosome with choline-related (e.g., Ralstonia solanacearum and Burkholderia xenovorans) or thiamin-related (e.g., Thermus thermophilus) genes, implying that they might encode transporters for these compounds. Radiometric uptake assays using Lactococcus lactis cells expressing NiaP proteins showed that B. subtilis, R. solanacearum, and B. xenovorans NiaP transport nicotinate via an energy-dependent mechanism. Likewise, NiaP proteins from maize (GRMZM2G381453, GRMZM2G066801, and GRMZM2G081774), Arabidopsis (At3g13050), and mouse (SVOP) transported nicotinate; the Arabidopsis protein also transported trigonelline. In contrast, T. thermophilus NiaP transported only thiamin. None of the proteins tested transported choline or the thiazole and pyrimidine products of thiamin breakdown. The maize and Arabidopsis NiaP proteins are the first nicotinate transporters reported in plants, the Arabidopsis protein is the first trigonelline transporter, and mouse SVOP appears to represent a novel type of mammalian nicotinate transporter. More generally, these results indicate that specificity for nicotinate is conserved widely, but not absolutely, among pro- and eukaryotic NiaP family proteins.

Original languageEnglish (US)
Pages (from-to)25-34
Number of pages10
JournalFunctional and Integrative Genomics
Volume12
Issue number1
DOIs
StatePublished - Mar 2012

Bibliographical note

Funding Information:
Acknowledgments This work was supported in part by US National Science Foundation award # IOS-1025398 (to A.D.H.), by Swiss National Science Foundation grant 31003A_127340 (to D.R.), and by an endowment from the C. V. Griffin, Sr. Foundation. The work of D. A.R. and A.L.O. was supported by the U.S. Department of Energy (DOE) Office of Biological and Environmental Research (BER), as part of BER’s Genomic Science Program (GSP) originating Foundational Scientific Focus Area (FSA) at the Pacific Northwest National Laboratory (PNNL). The work of D.A.R was also supported by award R01GM077402 from the National Institute of General Medical Sciences. We thank Dr. Edmund Kunji for his generous advice and encouragement, and M. Ziemak for technical support.

Keywords

  • Comparative genomics
  • Membrane transport
  • Nicotinate
  • Thiamin
  • Trigonelline

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