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Diversity of the metal-transporting P1B-type ATPases

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Abstract

The P1B-ATPases are integral membrane proteins that couple ATP hydrolysis to metal cation transport. Widely distributed across all domains of life, these enzymes have been previously shown to transport copper, zinc, cobalt, and other thiophilic heavy metals. Recent data suggest that these enzymes may also be involved in nickel and/or iron transport. Here we have exploited large amounts of genomic data to examine and classify the various P1B-ATPase subfamilies. Specifically, we have combined new methods of data partitioning and network visualization known as Transitivity Clustering and Protein Similarity Networks with existing biochemical data to examine properties such as length, speciation, and metal-binding motifs of the P1B-ATPase subfamily sequences. These data reveal interesting relationships among the enzyme sequences of previously established subfamilies, indicate the presence of two new subfamilies, and suggest the existence of new regulatory elements in certain subfamilies. Taken together, these findings underscore the importance of P1B-ATPases in homeostasis of nearly every biologically relevant transition metal and provide an updated framework for future studies.

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Abbreviations

AD:

Actuator domain

ATP:

Adenosine-5′-triphosphate

ATPBD:

ATP-binding domain

Fur:

Ferric uptake regulator

Hr:

Hemerythrin

MBD:

Metal-binding domain

ORF:

Open reading frame

SERCA:

Sarcoplasmic/endoplasmic reticulum Ca2+ transporter

TM:

Transmembrane helix

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Acknowledgments

This work was supported by National Institutes of Health Grants GM58518 (A.C.R.) and F32GM105339 (A.T.S.) and by the Walter S. and Lucienne Driskill Graduate Training Program in Life Sciences (K.P.S). Sequence searches utilized both database and analysis functions of the Universal Protein Resource (UniProt) Knowledgebase and Reference Clusters (http://www.unprot.org) and the National Center for Biotechnology Information (http://www.ncbi.nlm.nih.gov/).

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  1. Departments of Molecular Biosciences and of Chemistry, Northwestern University, 2205 Tech Drive, Evanston, IL, 60208, USA

    Aaron T. Smith, Kyle P. Smith & Amy C. Rosenzweig

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  1. Aaron T. Smith
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  2. Kyle P. Smith
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  3. Amy C. Rosenzweig
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Correspondence to Amy C. Rosenzweig.

Electronic supplementary material

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775_2014_1129_MOESM1_ESM.pdf

P1B-ATPase clustering data analyzed according to the length of the ATPase may be found as Fig. S1, and Uniprot accession numbers for the P1B-type ATPases and a list of their parent organisms used to generate all clustering networks in this work may be found as Table S1, both located in the electronic supplementary material. (PDF 709 kb)

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Smith, A.T., Smith, K.P. & Rosenzweig, A.C. Diversity of the metal-transporting P1B-type ATPases. J Biol Inorg Chem 19, 947–960 (2014). https://doi.org/10.1007/s00775-014-1129-2

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