Figure 4. Acyl-CoA synthetase activity of MbcS restores growth
of a S. aureus lpdA mbcS strain in rich, complex medium lacking
BCFAs.
(A) Clustal Omega (Sievers et al., 2011) was used to align MbcS
with amino acid sequences of previously characterized acyl-CoA
synthetases. Amino acids that constitute a conserved motif in the
C-terminal catalytic domain are shown. Amino acids strictly conserved in
the selected proteins are shaded; the conserved lysine residue required
for the catalytic activity of acyl-CoA synthetases is highlighted in
yellow. Acs, acetyl-CoA synthetase from Salmonella enterica(Starai & Escalante-Semerena, 2004); Acs2, acetyl-CoA synthetase fromSaccharomyces cerevisiae (Starai & Escalante-Semerena, 2004);
AcsA, acetyl-CoA synthetase from B. subtilis (Gardner et al.,
2006); IbuA, isobutyryl-CoA synthetase from R. palustrus (Crosby
& Escalante-Semerena, 2014; Crosby et al., 2012); FcsA, fatty acyl-CoA
synthetase from R. palustris (Crosby & Escalante-Semerena,
2014). (B) WT, mbcS, or lpdA mbcS strains
containing either the empty integration vector pCT3 (vector-only control
[VOC]), pCT3 containing the WT allele of S. aureus mbcS under
the control of the anhydrotetracycline inducible tet promoter
(pSambcS +), or the allele of mbcS that
codes for a lysine-to-alanine substitution at the residue 510
[pSambcS (K510A)] were grown in TSB and growth
(OD600) was monitored over time. (C, D) WT orlpdA mbcS strains with the empty vector control or the wild-type
allele of ibuA from R. palustris(pRpibuA +) (C) with or (D)without 25 ng ml-1 of anhydrotetracycline (aTc) as
gratuitous inducer were grown in TSB and OD600 was
monitored over time. Data are plotted as mean ± SD from three biological
replicates. **** p<0.0001, two-way ANOVA with Tukey’s
multiple comparison test. ns, not significant. In panel B, asterisks
indicate that lpdA mbcS VOC and lpdA
mbcS pSambcS (K510A) are statistically different
from WTVOC,mbcS VOC andlpdA mbcS pSambcS +. In panel C, asterisks
indicate that lpdA mbcS VOC and lpdA
mbcS pRpibuA + are statistically different from
WTVOC and mbcS VOC. In panel
D, asterisks indicate that lpdA mbcS VOC is
statistically different from WTVOC,mbcS VOC and lpdA
mbcS pRpibuA +.
Figure 5. MbcS is a methylbutyryl-CoA synthetase. (A)The activity of MbcS was tested in vitro with several short,
straight and branched carboxylic acids. Acids are indicated as
CX , where X denotes the carbon length.
Data are plotted as the mean specific activity of the enzyme ± SD of at
least three independent trials. (B) Sa MbcS was incubated
with 2.5 mM MgATP, 493 μM coenzyme A (CoA) and 73 μM isobutyric acid
(IB) to produce isobutyryl-CoA as described in Experimental
Procedures . Detection and quantification of CoA and IB-CoA was measured
via LC-MS. HK: heat killed enzyme. Traces are representative of three
independent trials.
Figure 6. S. aureus utilizes branched-chain aldehydes to
produce BCFAs in a MbcS-dependent manner . WT, lpdA mutant,lpdA mbcS1 suppressor mutant, and lpdA mbcS double mutant
cells were inoculated into chemically defined medium (CDM) (black) or
CDM supplemented with vehicle (DMSO; gray), i C4(2MB; pink), 2-methylbutyraldehyde (2MA; orange), and a 17:0 fatty
acid (green). Cell density (OD600) was measured after
overnight incubation (16-18 h of growth). Data are plotted as mean ± SD
from three biological replicates. **** p<0.0001,
***p<0.001, **p<0.01 two-way ANOVA with Tukey’s
multiple comparison test for each genotype; ns, not significant.
Figure 7. Metabolites from S. epidermidis support growth
of S. aureus in an MbcS-dependent manner. (A) The lpdAmutant (Left) and the lpdA mbcS double mutant (Right) were
inoculated ~5 mm apart from S. epidermidis on TSA
plates and incubated for 24 h. Arrow head indicates the point of
inoculation. (B) WT, lpdA mutant, and lpdA mbcS double
mutant cells were inoculated into chemically defined medium (CDM)
(black) or CDM supplemented with a mixture of a C5, i C4,
and i C5 (gray), a 17:0 fatty acid (orange), and 10%
(green), 1% (pink) or 0.1% (blue), of conditioned CDM from S.
epidermidis (i.e., cell-free supernatant). Cell density
(OD600) was measured after overnight incubation (16-18 h
of growth). Data are plotted as mean ± SD from three biological
replicates. **** p<0.0001, *p<0.05, two-way
ANOVA with Tukey’s multiple comparison test; ns, not significant.
Figure 8. Working model for the synthesis of BCFAs in S.
aureus in a BKDH-independent manner. In a lpdA mutant the BKDH
complex is inactive and during laboratory cultivation the synthesis of
BCFAs is blocked. S. aureus strains with high MbcS enzyme
activity (i.e., overexpression of mbcS ) can synthesize
BCFAs independent of the BKDH complex using exogenous or endogenous
precursors. We propose α-keto acids are converted into their respective
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reaction catalyzed by an aldehyde dehydrogenase to generate
branched-chain carboxylic acids. MbcS-dependent acyl-CoA synthesis feeds
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