Staphylococcus aureus SufT: an essential iron-sulphur cluster assembly factor in cells experiencing a high-demand for lipoic acid.
Staphylococcus aureus SufT is composed solely of the domain of unknown function 59 (DUF59) and has a role in the maturation of iron-sulphur (Fe-S) proteins. We report that SufT is essential for S. aureus when growth is heavily reliant upon lipoamide-utilizing enzymes, but dispensable when this reliance is decreased. LipA requires Fe-S clusters for lipoic acid (LA) synthesis and a ΔsufT strain had phenotypes suggestive of decreased LA production and decreased activities of lipoamide-requiring enzymes. Fermentative growth, a null clpC allele, or decreased flux through the TCA cycle diminished the demand for LA and rendered SufT non-essential. Abundance of the Fe-S cluster carrier Nfu was increased in a ΔclpC strain and a null clpC allele was unable to suppress the LA requirement of a ΔsufT Δnfu strain. Over-expression of nfu suppressed the LA requirement of the ΔsufT strain. We propose a model wherein SufT, and by extension the DUF59, is essential for the maturation of holo-LipA in S. aureus cells experiencing a high demand for lipoamide-dependent enzymes. The findings presented suggest that the demand for products of Fe-S enzymes is a factor governing the usage of one Fe-S cluster assembly factor over another in the maturation of apo-proteins.
Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, NJ, 08901, USA.
Ameya A
AA
Mashruwala
Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, NJ, 08901, USA.
Christina A
CA
Roberts
Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, NJ, 08901, USA.
Shiven
S
Bhatt
Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, NJ, 08901, USA.
Kerrie L
KL
May
Department of Cell Biology, Microbiology and Molecular Biology, University of South Florida, Tampa, FL, 33620, USA.
Ronan K
RK
Carroll
Department of Cell Biology, Microbiology and Molecular Biology, University of South Florida, Tampa, FL, 33620, USA.
Lindsey N
LN
Shaw
Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, NJ, 08901, USA.
Jeffrey M
JM
Boyd
D000154:Aconitate Hydratase / Q000378:metabolism; D001426:Bacterial Proteins / Q000378:metabolism; D002952:Citric Acid Cycle; D029968:Escherichia coli Proteins; D007501:Iron / Q000378:metabolism; D007506:Iron-Sulfur Proteins / Q000235:genetics / Q000378:metabolism*; D013203:Staphylococcal Infections; D013211:Staphylococcus aureus / Q000235:genetics / Q000378:metabolism*; D013455:Sulfur / Q000378:metabolism; D008063:Thioctic Acid / Q000031:analogs & derivatives / Q000235:genetics / Q000378:metabolism; D014157:Transcription Factors
D001426:Bacterial Proteins; D029968:Escherichia coli Proteins; D007506:Iron-Sulfur Proteins; C499695:IscR protein, E coli; C079999:LipA protein, Bacteria; D014157:Transcription Factors; D013455:Sulfur; D008063:Thioctic Acid; C013091:lipoamide; D007501:Iron; D000154:Aconitate Hydratase
Annu Rev Microbiol. 2006;60:533-59
16771650
J Microbiol Methods. 2014 May;100:46-51
24418681
Trends Genet. 2009 Aug;25(8):368-76
19665253
Science. 2003 Jan 31;299(5607):700-4
12560550
J Bacteriol. 2007 Jun;189(11):4275-89
17384184
J Bacteriol. 2003 Jan;185(1):221-30
12486059
J Bacteriol. 2005 Jul;187(13):4488-96
15968059
J Bacteriol. 2014 Dec;196(23):4140-51
25225270
Biochemistry. 2014 Jan 14;53(1):152-60
24321018
J Bacteriol. 2009 Apr;191(7):2187-96
19181817
Nat Struct Biol. 2001 Mar;8(3):230-3
11224567
Nature. 1983 Oct 20-26;305(5936):709-12
6226876
Proteomics. 2009 Mar;9(5):1152-76
19253280
Infect Immun. 2010 Apr;78(4):1618-28
20100857
J Biol Chem. 2001 Aug 3;276(31):29420-9
11346657
Mol Microbiol. 2002 Mar;43(6):1387-400
11952893
Plant J. 2004 Jan;37(2):174-85
14690502
Arch Microbiol. 1990;154(1):50-5
2118752
mBio. 2014 Sep 02;5(5):e01729-14
25182329
Infect Immun. 2002 Nov;70(11):6373-82
12379717
J Biol Chem. 1952 Mar;195(1):133-40
14938361
J Am Chem Soc. 2005 Mar 9;127(9):2860-1
15740115
Methods Enzymol. 1991;204:587-636
1658572
Int J Med Microbiol. 2011 Apr;301(4):341-6
21273120
Appl Environ Microbiol. 2013 Apr;79(7):2218-24
23354696
Plant Cell. 2012 Oct;24(10):4135-48
23104832
Proc Natl Acad Sci U S A. 1964 Apr;51:585-92
14166766
Cell Metab. 2013 Aug 6;18(2):187-98
23891004
Mol Gen Genet. 1989 Dec;220(1):154-6
2691872
Proc Natl Acad Sci U S A. 2009 May 19;106(20):8344-9
19416816
Arch Microbiol. 2005 May;183(4):286-91
15843987
Curr Genet. 2016 Feb;62(1):59-65
26259870
mBio. 2013 Feb 12;4(1):e00537-12
23404398
J Microbiol Methods. 2007 Jul;70(1):186-90
17512993
Biochem J. 2014 Nov 15;464(1):123-33
25100160
J Bacteriol. 1997 Jun;179(12):3989-96
9190816
J Innate Immun. 2010;2(6):546-59
20829608
J Am Chem Soc. 2015 Oct 21;137(41):13216-9
26390103
J Bacteriol. 1973 May;114(2):563-70
4574693
Mol Microbiol. 2015 Feb;95(3):383-409
25388433
PLoS Genet. 2009 May;5(5):e1000497
19478995
FEMS Microbiol Lett. 1994 Apr 1;117(2):163-8
8181719
J Bacteriol. 2014 Jun;196(12):2178-89
24706736
Mol Gen Genet. 1983;192(1-2):15-20
6358793
Mol Microbiol. 1999 Jan;31(1):79-87
9987112
Biochem J. 2009 Dec 14;425(1):207-14
19817716
Eukaryot Cell. 2014 Jan;13(1):143-53
24243793
Antimicrob Agents Chemother. 2013 Jul;57(7):3283-92
23629700
Nat Rev Microbiol. 2010 Jun;8(6):436-46
20467446
Biochemistry. 2010 Oct 12;49(40):8794-802
20822158
J Biol Chem. 1991 Oct 15;266(29):19328-33
1655783
Acta Crystallogr D Biol Crystallogr. 2012 Jun;68(Pt 6):637-48
22683786
Annu Rev Microbiol. 2011;65:129-47
21639791
Biochem Biophys Res Commun. 1981 Aug 31;101(4):1372-80
7306136
Microbiologyopen. 2014 Aug;3(4):497-512
24931910
FEBS Lett. 1999 Jun 18;453(1-2):25-8
10403368
Methods Mol Biol. 2016;1373:33-41
26194707
Mol Microbiol. 2010 Dec;78(6):1448-67
21143317
Mol Microbiol. 2015 Oct;98(2):218-42
26135358
Mol Microbiol. 2003 Jun;48(6):1565-78
12791139
PLoS Genet. 2016 Aug 12;12(8):e1006233
27517714
PLoS One. 2010 Apr 14;5(4):e10146
20418950
J Bacteriol. 2010 Mar;192(5):1459-62
20061474
Proc Natl Acad Sci U S A. 2016 Aug 23;113(34):9446-50
27506792
Proc Natl Acad Sci U S A. 2005 Mar 1;102(9):3266-71
15728363
J Microbiol Methods. 2009 Jun;77(3):251-60
19264102
Microbiology (Reading). 2006 Aug;152(Pt 8):2345-2353
16849799
Nature. 2010 Dec 9;468(7325):790-5
21085121