title: Loose coupling in the bacterial flagellar motor.
abstract: Physiological properties of the flagellar rotary motor have been taken to indicate a tightly coupled mechanism in which each revolution is driven by a fixed number of energizing ions. Measurements that would directly test the tight-coupling hypothesis have not been made. Energizing ions flow through membrane-bound complexes formed from the proteins MotA and MotB, which are anchored to the cell wall and constitute the stator. Genetic and biochemical evidence points to a "power stroke" mechanism in which the ions interact with an aspartate residue of MotB to drive conformational changes in MotA that are transmitted to the rotor protein FliG. Each stator complex contains two separate ion-binding sites, raising the question of whether the power stroke is driven by one, two, or either number of ions. Here, we describe simulations of a model in which the conformational change can be driven by either one or two ions. This loosely coupled model can account for the observed physiological properties of the motor, including those that have been taken to indicate tight coupling; it also accords with recent measurements of motor torque at high load that are harder to explain in tight-coupling models. Under loads relevant to a swimming cell, the loosely coupled motor would perform about as well as a two-proton motor and significantly better than a one-proton motor. The loosely coupled motor is predicted to be especially advantageous under conditions of diminished energy supply, or of reduced temperature, turning faster than an obligatorily two-proton motor while using fewer ions.
authors.affiliation: Department of Biology, University of Utah, Salt Lake City, UT 84112.
authors.forename: Ryan
authors.initials: R
authors.lastname: Boschert
authors.affiliation: Department of Biology, University of Utah, Salt Lake City, UT 84112.
authors.forename: Frederick R
authors.initials: FR
authors.lastname: Adler
authors.affiliation: Department of Biology, University of Utah, Salt Lake City, UT 84112 blair@bioscience.utah.edu.
authors.forename: David F
authors.initials: DF
authors.lastname: Blair
mesh_terms: D001224:Aspartic Acid / Q000737:chemistry / Q000378:metabolism; D001426:Bacterial Proteins / Q000737:chemistry / Q000378:metabolism*; D001665:Binding Sites; D002462:Cell Membrane / Q000378:metabolism; D005407:Flagella / Q000378:metabolism* / Q000502:physiology; D007477:Ions / Q000737:chemistry / Q000378:metabolism; D007700:Kinetics; D008954:Models, Biological; D008958:Models, Molecular; D020409:Molecular Motor Proteins / Q000737:chemistry / Q000378:metabolism*; D009068:Movement / Q000502:physiology; D011485:Protein Binding; D011487:Protein Conformation; D011522:Protons; D012399:Rotation; D012964:Sodium / Q000737:chemistry / Q000378:metabolism; D013696:Temperature; D019415:Torque
chemical_list: D001426:Bacterial Proteins; C075660:Flig protein, Bacteria; D007477:Ions; D020409:Molecular Motor Proteins; C063010:MotA protein, Bacteria; C064779:MotB protein, Bacteria; D011522:Protons; D001224:Aspartic Acid; D012964:Sodium
keywords: bioenergetics; kinetic analysis; molecular machines; motility
references.citation: Biophys J. 2000 Feb;78(2):1036-41
references.pmid: 10653817
references.citation: J Biol Chem. 2000 Feb 25;275(8):5718-22
references.pmid: 10681557
references.citation: J Bacteriol. 2001 Nov;183(21):6404-12
references.pmid: 11591685
references.citation: Biochemistry. 2001 Oct 30;40(43):13041-50
references.pmid: 11669642
references.citation: Biochemistry. 2001 Oct 30;40(43):13051-9
references.pmid: 11669643
references.citation: Biophys J. 2003 Jan;84(1):571-7
references.pmid: 12524310
references.citation: Proc Natl Acad Sci U S A. 2003 Jul 22;100(15):8748-51
references.pmid: 12857945
references.citation: Science. 1988 Jan 15;239(4837):276-8
references.pmid: 2447650
references.citation: Cell. 1987 Jun 5;49(5):643-50
references.pmid: 3034430
references.citation: Adv Biophys. 1986;22:151-83
references.pmid: 2882655
references.citation: Nature. 1984 May 31-Jun 6;309(5967):470-2
references.pmid: 6374467
references.citation: Cell. 1983 Mar;32(3):913-9
references.pmid: 6831561
references.citation: J Mol Biol. 1980 Apr 15;138(3):541-61
references.pmid: 7411617
references.citation: Proc Natl Acad Sci U S A. 1974 Apr;71(4):1239-43
references.pmid: 4598295
references.citation: J Biochem. 2004 Jan;135(1):43-51
references.pmid: 14999008
references.citation: Annu Rev Biochem. 2003;72:19-54
references.pmid: 12500982
references.citation: Biochemistry. 2004 Jan 13;43(1):26-34
references.pmid: 14705928
references.citation: Biochemistry. 2004 Jan 13;43(1):35-45
references.pmid: 14705929
references.citation: J Mol Biol. 1988 Aug 5;202(3):575-84
references.pmid: 3050128
references.citation: Science. 1988 Dec 23;242(4886):1678-81
references.pmid: 2849208
references.citation: Biophys J. 1989 May;55(5):905-14
references.pmid: 2720081
references.citation: Cell. 1990 Feb 9;60(3):439-49
references.pmid: 2154333
references.citation: Biophys J. 1990 Apr;57(4):779-96
references.pmid: 2160845
references.citation: Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6304-8
references.pmid: 1631122
references.citation: J Mol Biol. 1995 Aug 11;251(2):237-42
references.pmid: 7643400
references.citation: J Bacteriol. 1997 Aug;179(16):5104-10
references.pmid: 9260952
references.citation: J Bacteriol. 1998 May;180(10):2729-35
references.pmid: 9573160
references.citation: Proc Natl Acad Sci U S A. 1998 May 26;95(11):6436-41
references.pmid: 9600984
references.citation: Biophys J. 1999 Jan;76(1 Pt 1):580-7
references.pmid: 9876171
references.citation: Nature. 2005 Oct 6;437(7060):916-9
references.pmid: 16208378
references.citation: J Bacteriol. 2006 Feb;188(4):1466-72
references.pmid: 16452430
references.citation: Proc Natl Acad Sci U S A. 2006 May 23;103(21):8066-71
references.pmid: 16698936
references.citation: Nature. 2006 Sep 21;443(7109):355-8
references.pmid: 16971952
references.citation: J Bacteriol. 2006 Oct;188(20):7039-48
references.pmid: 17015643
references.citation: J Bacteriol. 2007 Mar;189(5):1756-64
references.pmid: 17189361
references.citation: Proc Natl Acad Sci U S A. 2008 Jul 29;105(30):10348-53
references.pmid: 18647830
references.citation: Biochemistry. 2008 Oct 28;47(43):11332-9
references.pmid: 18834143
references.citation: Mol Microbiol. 2008 Dec;70(6):1397-407
references.pmid: 19019148
references.citation: Proc Natl Acad Sci U S A. 2013 Jul 9;110(28):E2544-51
references.pmid: 23788659
references.citation: J Bacteriol. 2014 Apr;196(7):1377-85
references.pmid: 24464458
references.citation: Proc Natl Acad Sci U S A. 2013 Jul 16;110(29):11839-44
references.pmid: 23818629
references.citation: J Biol Chem. 2012 Oct 19;287(43):35779-83
references.pmid: 22896702
references.citation: J Mol Biol. 2012 Feb 17;416(2):192-207
references.pmid: 22210351
references.citation: EMBO J. 2011 Jul 20;30(14):2962-71
references.pmid: 21673656
references.citation: Proc Natl Acad Sci U S A. 2010 Oct 12;107(41):17616-20
references.pmid: 20876126
references.citation: Nature. 2010 Aug 19;466(7309):996-1000
references.pmid: 20676082
references.citation: PLoS Comput Biol. 2009 Oct;5(10):e1000540
references.pmid: 19851449
references.citation: Biochemistry. 2009 Dec 15;48(49):11699-705
references.pmid: 19894756
references.citation: Biophys J. 2010 May 19;98(10):2121-6
references.pmid: 20483319