Electron Accepting Units of the Diheme Cytochrome c TsdA, a Bifunctional Thiosulfate Dehydrogenase/Tetrathionate Reductase.
The enzymes of the thiosulfate dehydrogenase (TsdA) family are wide-spread diheme c-type cytochromes. Here, redox carriers were studied mediating the flow of electrons arising from thiosulfate oxidation into respiratory or photosynthetic electron chains. In a number of organisms, including Thiomonas intermedia and Sideroxydans lithotrophicus, the tsdA gene is immediately preceded by tsdB encoding for another diheme cytochrome. Spectrophotometric experiments in combination with enzymatic assays in solution showed that TsdB acts as an effective electron acceptor of TsdA in vitro when TsdA and TsdB originate from the same source organism. Although TsdA covers a range from -300 to +150 mV, TsdB is redox active between -100 and +300 mV, thus enabling electron transfer between these hemoproteins. The three-dimensional structure of the TsdB-TsdA fusion protein from the purple sulfur bacterium Marichromatium purpuratum was solved by X-ray crystallography to 2.75 Å resolution providing insights into internal electron transfer. In the oxidized state, this tetraheme cytochrome c contains three hemes with axial His/Met ligation, whereas heme 3 exhibits the His/Cys coordination typical for TsdA active sites. Interestingly, thiosulfate is covalently bound to Cys330on heme 3. In several bacteria, including Allochromatium vinosum, TsdB is not present, precluding a general and essential role for electron flow. Both AvTsdA and the MpTsdBA fusion react efficiently in vitro with high potential iron-sulfur protein from A. vinosum (Em+350 mV). High potential iron-sulfur protein not only acts as direct electron donor to the reaction center in anoxygenic phototrophs but can also be involved in aerobic respiratory chains.
From the Institut für Mikrobiologie & Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, 53115 Bonn, Germany.
Julia M
http://orcid.org/0000-0002-1221-1230
JM
Kurth
the Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa (ITQB-UNL), 2780-157 Oeiras, Portugal, and.
José A
JA
Brito
From the Institut für Mikrobiologie & Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, 53115 Bonn, Germany.
Jula
J
Reuter
From the Institut für Mikrobiologie & Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, 53115 Bonn, Germany.
Alexander
A
Flegler
From the Institut für Mikrobiologie & Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, 53115 Bonn, Germany.
Tobias
T
Koch
From the Institut für Mikrobiologie & Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, 53115 Bonn, Germany.
Thomas
T
Franke
From the Institut für Mikrobiologie & Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, 53115 Bonn, Germany.
Eva-Maria
EM
Klein
the Centre for Molecular and Structural Biochemistry, School of Chemistry and School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, United Kingdom.
Sam F
SF
Rowe
the Centre for Molecular and Structural Biochemistry, School of Chemistry and School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, United Kingdom.
Julea N
http://orcid.org/0000-0002-9624-5226
JN
Butt
From the Institut für Mikrobiologie & Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, 53115 Bonn, Germany.
Kevin
K
Denkmann
the Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa (ITQB-UNL), 2780-157 Oeiras, Portugal, and.
Inês A C
http://orcid.org/0000-0003-3283-4520
IA
Pereira
the Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa (ITQB-UNL), 2780-157 Oeiras, Portugal, and archer@itqb.unl.pt.
Margarida
http://orcid.org/0000-0001-8419-5420
M
Archer
From the Institut für Mikrobiologie & Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, 53115 Bonn, Germany, chdahl@uni-bonn.de.
Christiane
http://orcid.org/0000-0001-8288-7546
C
Dahl
D001419:Bacteria / Q000201:enzymology* / Q000235:genetics; D001426:Bacterial Proteins / Q000737:chemistry* / Q000235:genetics; D018360:Crystallography, X-Ray; D010088:Oxidoreductases / Q000737:chemistry* / Q000235:genetics
D001426:Bacterial Proteins; D010088:Oxidoreductases; C022727:tetrathionate reductase; C432587:thiosulfate dehydrogenase
TsdA; crystal structure; cytochrome c; electron acceptor; enzyme kinetics; heme; protein chemistry; respiratory chain; thiosulfate dehydrogenase
Environ Microbiol. 2012 Oct;14(10):2673-88
22779704
J Bacteriol. 2014 Dec;196(24):4206-15
25182500
Biochim Biophys Acta. 1997 May 2;1352(1):18-22
9177478
J Biol Chem. 2015 Apr 3;290(14):9222-38
25673691
Front Microbiol. 2015 Apr 28;6:332
25972843
Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501
20383002
J Mol Biol. 1983 Jun 5;166(4):557-80
6345791
Acta Crystallogr D Biol Crystallogr. 2013 Jul;69(Pt 7):1204-14
23793146
Biochemistry. 2002 Jul 16;41(28):8868-75
12102629
J Bacteriol. 1995 Feb;177(3):608-13
7836293
Acta Crystallogr D Biol Crystallogr. 2006 Jan;62(Pt 1):72-82
16369096
EMBO J. 2002 Nov 1;21(21):5599-610
12411478
Acta Crystallogr D Biol Crystallogr. 2010 Jan;66(Pt 1):12-21
20057044
Biochim Biophys Acta. 1999 Jan 27;1410(1):51-60
10076014
Methods Enzymol. 1997;276:472-494
27799110
Arch Microbiol. 1996 Dec;166(6):372-8
9082913
Acta Crystallogr D Biol Crystallogr. 2012 Apr;68(Pt 4):352-67
22505256
J Am Chem Soc. 2008 Jul 9;130(27):8588-9
18549208
Nat Struct Biol. 1997 Apr;4(4):276-84
9095195
Biophys J. 1972 Jul;12(7):882-96
5037342
Methods Enzymol. 1978;53:329-40
713842
J Mol Biol. 1968 Apr 28;33(2):491-7
5700707
Biochemistry. 2007 Jul 3;46(26):7804-10
17547421
Proteins. 2003 Feb 15;50(3):437-50
12557186
Biochim Biophys Acta. 1969 Oct 21;189(2):245-55
5350450
Science. 2012 May 25;336(6084):1030-3
22628654
Biochim Biophys Acta. 1993 Sep 3;1202(1):82-6
8396977
J Biol Chem. 2008 Aug 8;283(32):22206-14
18552405
Acta Crystallogr D Biol Crystallogr. 2011 Apr;67(Pt 4):282-92
21460446
Biochemistry. 2009 Sep 29;48(38):9132-9
19697907
Biochemistry. 2002 Nov 26;41(47):14028-32
12437360
Appl Environ Microbiol. 2015 Sep 1;81(17):5927-37
26092463
Biochim Biophys Acta. 2003 Mar 6;1557(1-3):83-90
12615351
Coord Chem Rev. 2011 Apr 1;255(7-8):700-716
21423881
J Biol Chem. 2012 Nov 23;287(48):40350-9
23060437
Biochemistry. 2010 Sep 7;49(35):7494-503
20715760
Arch Biochem Biophys. 2007 Nov 15;467(2):174-84
17931594
J Mol Biol. 2008 Dec 31;384(5):1287-300
18952098
Nucleic Acids Res. 2010 Jul;38(Web Server issue):W545-9
20457744
Biochem Biophys Res Commun. 1998 Oct 29;251(3):744-7
9790980
J Am Chem Soc. 2015 Oct 21;137(41):13232-5
26437022
Nat Struct Biol. 1999 Dec;6(12):1108-12
10581550
Mol Microbiol. 2013 Apr;88(1):173-88
23421726
Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2210-21
15572774
Acta Crystallogr D Biol Crystallogr. 2011 Apr;67(Pt 4):293-302
21460447
Biochemistry. 2006 Jan 10;45(1):249-62
16388601
Biochim Biophys Acta. 1991 May 23;1058(1):28-30
2043646
J Biol Chem. 2011 Jul 15;286(28):24872-81
21592966
J Struct Biol. 2005 Dec;152(3):229-34
16297640
Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):125-32
20124692
J Biol Chem. 2015 Apr 3;290(14):9209-21
25673696
Methods Mol Biol. 2007;364:215-30
17172768