Evolutionary relationships of ATP-Binding Cassette (ABC) uptake porters

BMC Microbiology

Milton H Saier⁴  Eric I Sun⁵  Vamsee Reddy³  Maksim A Shlykov¹  Åke Västermark⁴  Wei Hao Zheng² 

[1]Present address: University of Michigan Medical School, Ann Arbor, MI, USA

[2]Present address: Medical College of Wisconsin, Milwaukee, WI, USA

[3]Present address: University of Calgary, Calgary, AB, Canada

[4]Department of Molecular Biology, University of California at San Diego, La Jolla, CA, 92093-0116, USA

[5]Present address: Burnham Institute, La Jolla, CA, USA

关键词: Comparisons;    Protein superfamilies;    Membranes;    Transport proteins;    Uptake;    ABC;    ATP-Binding Cassette;   

Others  :  1143762
DOI  :  10.1186/1471-2180-13-98

 received in 2012-10-29, accepted in 2013-04-19,  发布年份 2013

【 摘 要 】

Background

The ATP-Binding Cassette (ABC) functional superfamily includes integral transmembrane exporters that have evolved three times independently, forming three families termed ABC1, ABC2 and ABC3, upon which monophyletic ATPases have been superimposed for energy-coupling purposes [e.g., J Membr Biol 231(1):1-10, 2009]. The goal of the work reported in this communication was to understand how the integral membrane constituents of ABC uptake transporters with different numbers of predicted or established transmembrane segments (TMSs) evolved. In a few cases, high resolution 3-dimensional structures were available, and in these cases, their structures plus primary sequence analyses allowed us to predict evolutionary pathways of origin.

Results

All of the 35 currently recognized families of ABC uptake proteins except for one (family 21) were shown to be homologous using quantitative statistical methods. These methods involved using established programs that compare native protein sequences with each other, after having compared each sequence with thousands of its own shuffled sequences, to gain evidence for homology. Topological analyses suggested that these porters contain numbers of TMSs ranging from four or five to twenty. Intragenic duplication events occurred multiple times during the evolution of these porters. They originated from a simple primordial protein containing 3 TMSs which duplicated to 6 TMSs, and then produced porters of the various topologies via insertions, deletions and further duplications. Except for family 21 which proved to be related to ABC1 exporters, they are all related to members of the previously identified ABC2 exporter family. Duplications that occurred in addition to the primordial 3 → 6 duplication included 5 → 10, 6 → 12 and 10 → 20 TMSs. In one case, protein topologies were uncertain as different programs gave discrepant predictions. It could not be concluded with certainty whether a 4 TMS ancestral protein or a 5 TMS ancestral protein duplicated to give an 8 or a 10 TMS protein. Evidence is presented suggesting but not proving that the 2TMS repeat unit in ABC1 porters derived from the two central TMSs of ABC2 porters. These results provide structural information and plausible evolutionary pathways for the appearance of most integral membrane constituents of ABC uptake transport systems.

Conclusions

Almost all integral membrane uptake porters of the ABC superfamily belong to the ABC2 family, previously established for exporters. Most of these proteins can have 5, 6, 10, 12 or 20 TMSs per polypeptide chain. Evolutionary pathways for their appearance are proposed.

【 授权许可】

   
2013 Zheng et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 9.

Figure 10.

Figure 11.

Figure 12.

Figure 13.

Figure 14.

【 参考文献 】

• [1]Wang B, Dukarevich M, Sun EI, Yen MR, Saier MH Jr: Membrane porters of ATP-binding cassette transport systems are polyphyletic. J Membr Biol 2009, 231(1):1-10.
• [2]Busch W, Saier MH Jr: The transporter classification (TC) system, 2002. Crit Rev Biochem Mol Biol 2002, 37(5):287-337.
• [3]Saier MH Jr, Tran CV, Barabote RD: TCDB: the transporter classification database for membrane transport protein analyses and information. Nucleic Acids Res 2006, 34(Database issue):D181-D186.
• [4]Thever MD, Saier MH Jr: Bioinformatic characterization of p-type ATPases encoded within the fully sequenced genomes of 26 eukaryotes. J Membr Biol 2009, 229(3):115-130.
• [5]Saurin W, Hofnung M, Dassa E: Getting in or out: early segregation between importers and exporters in the evolution of ATP-binding cassette (ABC) transporters. J Mol Evol 1999, 48(1):22-41.
• [6]Hvorup RN, Goetz BA, Niederer M, Hollenstein K, Perozo E, Locher KP: Asymmetry in the structure of the ABC transporter-binding protein complex BtuCD-BtuF. Science 2007, 317(5843):1387-1390.
• [7]Oldham ML, Khare D, Quiocho FA, Davidson AL, Chen J: Crystal structure of a catalytic intermediate of the maltose transporter. Nature 2007, 450(7169):515-521.
• [8]Biemans-Oldehinkel E, Poolman B: On the role of the two extracytoplasmic substrate-binding domains in the ABC transporter OpuA. EMBO J 2003, 22(22):5983-5993.
• [9]Tam R, Saier MH Jr: Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev 1993, 57(2):320-346.
• [10]Eitinger T, Rodionov DA, Grote M, Schneider E: Canonical and ECF-type ATP-binding cassette importers in prokaryotes: diversity in modular organization and cellular functions. FEMS Microbiol Rev 2011, 35(1):3-67.
• [11]Rodionov DA, Hebbeln P, Eudes A, ter Beek J, Rodionova IA, Erkens GB, Slotboom DJ, Gelfand MS, Osterman AL, Hanson AD: A novel class of modular transporters for vitamins in prokaryotes. J Bacteriol 2009, 191(1):42-51.
• [12]Khwaja M, Ma Q, Saier MH Jr: Topological analysis of integral membrane constituents of prokaryotic ABC efflux systems. Res Microbiol 2005, 156(2):270-277.
• [13]Yen MR, Choi J, Saier MH Jr: Bioinformatic analyses of transmembrane transport: novel software for deducing protein phylogeny, topology, and evolution. J Mol Microbiol Biotechnol 2009, 17(4):163-176.
• [14]Zhai Y, Saier MH Jr: A simple sensitive program for detecting internal repeats in sets of multiply aligned homologous proteins. J Mol Microbiol Biotechnol 2002, 4(4):375-377.
• [15]Zhou X, Yang NM, Tran CV, Hvorup RN, Saier MH Jr: Web-based programs for the display and analysis of transmembrane alpha-helices in aligned protein sequences. J Mol Microbiol Biotechnol 2003, 5(1):1-6.
• [16]Reddy VS, Saier MH Jr: BioV Suite–a collection of programs for the study of transport protein evolution. FEBS J 2012, 279(11):2036-2046.
• [17]Doolittle RF: Similar amino acid sequences: chance or common ancestry? Science 1981, 214(4517):149-159.
• [18]Saier MH Jr: Computer-aided analyses of transport protein sequences: gleaning evidence concerning function, structure, biogenesis, and evolution. Microbiol Rev 1994, 58(1):71-93.
• [19]Saier MH Jr: Tracing pathways of transport protein evolution. Mol Microbiol 2003, 48(5):1145-1156.
• [20]Tran CV, Saier MH Jr: The principal chloroquine resistance protein of Plasmodium falciparum is a member of the drug/metabolite transporter superfamily. Microbiology 2004, 150(Pt 1):1-3.
• [21]Yen MR, Chen JS, Marquez JL, Sun EI, Saier MH: Multidrug resistance: phylogenetic characterization of superfamilies of secondary carriers that include drug exporters. Methods Mol Biol 2010, 637:47-64.
• [22]Gomolplitinant KM, Saier MH Jr: Evolution of the oligopeptide transporter family. J Membr Biol 2011, 240(2):89-110.
• [23]Nelson RD, Kuan G, Saier MH Jr, Montal M: Modular assembly of voltage-gated channel proteins: a sequence analysis and phylogenetic study. J Mol Microbiol Biotechnol 1999, 1(2):281-287.
• [24]Li W, Godzik A: Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006, 22(13):1658-1659.
• [25]Zhai Y, Saier MH Jr: A web-based program (WHAT) for the simultaneous prediction of hydropathy, amphipathicity, secondary structure and transmembrane topology for a single protein sequence. J Mol Microbiol Biotechnol 2001, 3(4):501-502.
• [26]Bernsel A, Viklund H, Hennerdal A, Elofsson A: TOPCONS: consensus prediction of membrane protein topology. Nucleic Acids Res 2009, 37(Web Server issue):W465-W468.
• [27]Schultz-Hauser G, Koster W, Schwarz H, Braun V: Iron(III) hydroxamate transport in Escherichia coli K-12: FhuB-mediated membrane association of the FhuC protein and negative complementation of fhuC mutants. J Bacteriol 1992, 174(7):2305-2311.
• [28]Bogdanov M, Xie J, Dowhan W: Lipid-protein interactions drive membrane protein topogenesis in accordance with the positive inside rule. J Biol Chem 2009, 284(15):9637-9641.
• [29]Tusnady GE, Simon I: The HMMTOP transmembrane topology prediction server. Bioinformatics 2001, 17(9):849-850.
• [30]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23(21):2947-2948.
• [31]Pinkett HW, Lee AT, Lum P, Locher KP, Rees DC: An inward-facing conformation of a putative metal-chelate-type ABC transporter. Science 2007, 315(5810):373-377.
• [32]Kadaba NS, Kaiser JT, Johnson E, Lee A, Rees DC: The high-affinity E. coli methionine ABC transporter: structure and allosteric regulation. Science 2008, 321(5886):250-253.
• [33]Gerber S, Comellas-Bigler M, Goetz BA, Locher KP: Structural basis of trans-inhibition in a molybdate/tungstate ABC transporter. Science 2008, 321(5886):246-250.
• [34]Nguyen TX, Yen MR, Barabote RD, Saier MH Jr: Topological predictions for integral membrane permeases of the phosphoenolpyruvate:sugar phosphotransferase system. J Mol Microbiol Biotechnol 2006, 11(6):345-360.
• [35]Devereux J, Haeberli P, Smithies O: A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 1984, 12(1 Pt 1):387-395.
• [36]Dayhoff MO, Barker WC, Hunt LT: Establishing homologies in protein sequences. Methods Enzymol 1983, 91:524-545.
• [37]Zhai Y, Saier MH Jr: A web-based program for the prediction of average hydropathy, average amphipathicity and average similarity of multiply aligned homologous proteins. J Mol Microbiol Biotechnol 2001, 3(2):285-286.
• [38]Krogh A, Larsson B, von Heijne G, Sonnhammer EL: Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001, 305(3):567-580.
• [39]Cai W, Pei J, Grishin NV: Reconstruction of ancestral protein sequences and its applications. BMC Evol Biol 2004, 4:33. BioMed Central Full Text