Substrate specificities and expression patterns reflect the evolutionary divergence of maltose ABC transporters in Thermotoga maritima.
Duplication of transporter genes is apparent in the genome sequence of the hyperthermophilic bacterium Thermotoga maritima. The physiological impacts of these duplications are not well understood, so we used the bacterium's two putative maltose transporters to begin a study of the evolutionary relationship between a transporter's function and the control of expression of its genes. We show that the substrate binding proteins encoded by these operons, MalE1 and MalE2, have different substrate specificities and affinities and that they are expressed under different growth conditions. MalE1 binds maltose (dissociation constant [KD], 24 +/- 1 microM), maltotriose (KD, 8 +/- 0.5 nM), and beta-(1-->4)-mannotetraose (KD, 38 +/- 1 microM). In contrast, MalE2 binds maltose (KD, 8.4 +/- 1 microM), maltotriose (KD, 11.5 +/- 1.5 microM), and trehalose (KD, 9.5 +/- 1.0 microM) confirming the findings of Wassenberg et al. (J. Mol. Biol. 295:279-288, 2000). Neither protein binds lactose. We examined the expression of these operons at both the transcriptional and translational levels and found that MalE1 is expressed in cells grown on lactose or guar gum and that MalE2 is highly expressed in starch- and trehalose-grown cells. Evidence is provided that malE1, malF1, and perhaps malG1 are cotranscribed and so constitute an operon. An open reading frame encoding a putative transcriptional regulatory protein adjacent to this operon (TM1200) is also up-regulated in response to growth on lactose. These evolutionarily related transporter operons have diverged both in function and expression to assume apparently different physiological roles.
Nanavati
Dhaval M
DM
Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269-3125, USA.
Nguyen
Tu N
TN
Noll
Kenneth M
KM
D018528:ATP-Binding Cassette Transporters / Q000235:genetics* / Q000378:metabolism*; D019143:Evolution, Molecular; D015964:Gene Expression Regulation, Bacterial; D008320:Maltose / Q000378:metabolism*; D009876:Operon / Q000235:genetics; D014176:Protein Biosynthesis; D020124:Thermotoga maritima / Q000235:genetics* / Q000378:metabolism*; D014158:Transcription, Genetic
D018528:ATP-Binding Cassette Transporters; D008320:Maltose
Cell. 1987 Dec 24;51(6):1131-43
2446776
Cell. 1987 Jan 30;48(2):297-310
2433046
Anal Biochem. 1989 Nov 1;182(2):319-26
2610349
J Mol Biol. 1993 Apr 5;230(3):800-11
8478935
Microbiol Rev. 1993 Jun;57(2):320-46
8336670
J Bacteriol. 1994 Aug;176(16):5033-43
8051015
Mol Microbiol. 1996 Apr;20(1):17-25
8861200
Protein Eng. 1997 Jan;10(1):1-6
9051728
Methods Enzymol. 1997;278:221-57
9170316
Mol Microbiol. 1998 Aug;29(3):685-94
9723909
J Bacteriol. 1998 Sep;180(18):4893-902
9733693
Nature. 1999 May 27;399(6734):323-9
10360571
Archaea. 2002 Mar;1(1):19-25
15803655
J Mol Biol. 2000 Jan 14;295(2):279-88
10623526
Nucleic Acids Res. 2000 Feb 1;28(3):706-9
10637321
Extremophiles. 2000 Aug;4(4):189-200
10972187
J Bacteriol. 2000 Nov;182(22):6292-301
11053372
Mol Microbiol. 2000 Nov;38(4):684-93
11115105
Methods Enzymol. 2001;330:169-80
11210497
Biotechnol Bioeng. 2001 Nov 5;75(3):322-33
11590605
J Bacteriol. 2002 Aug;184(16):4475-88
12142418
Microbiology. 2002 Nov;148(Pt 11):3531-7
12427944
J Biol Chem. 2003 Jan 10;278(2):983-90
12426307
J Biol Chem. 2003 Feb 28;278(9):7540-52
12475972
Mol Biol Evol. 2003 Feb;20(2):267-77
12598694
Nat Genet. 2004 May;36(5):492-6
15107850
Biochem Biophys Res Commun. 2004 Jun 18;319(1):230-4
15158466
J Bacteriol. 2004 Jul;186(14):4824-8
15231816
Nature. 1970 Aug 15;227(5259):680-5
5432063
J Biol Chem. 1972 Feb 10;247(3):917-24
4550764
Anal Biochem. 1976 May 7;72:248-54
942051
Mol Microbiol. 1988 Jan;2(1):141-52
3130541