Peptide transport is a crucial step in the growth of Streptococcus thermophilus in protein- or peptide-containing media. The objective of the present work was to determine the specificity of peptide utilization by this widely used lactic acid bacterium. To reach that goal, complementary approaches were employed. The capability of a proteinase-negative S. thermophilus strain to grow in a chemically defined medium containing a mixture of peptides isolated from milk as the source of amino acids was analysed. Peptides were separated into three size classes by ultrafiltration. The strain was able to use peptides up to 3·5 kDa during growth, as revealed by liquid chromatography and mass spectrometry analyses. The same strain was grown in chemically defined medium containing a tryptic digest of casein, and the respective time-course consumption of the peptides during growth was estimated. The ability to consume large peptides (up to 23 residues) was confirmed, as long as they are cationic and hydrophobic. These results were confirmed by peptide transport studies. Extension of the study to 11 other strains revealed that they all shared these preferences.
AlloingG., de PhillipP.,
ClaverysJ.-P.
1994; Three highly homologous membrane-bound lipoproteins participate in oligopeptide transport by the ami system of gram-positive Streptococcus pneumoniae. J Mol Biol 241:44–58[CrossRef]
BellengierP.,
RichardJ.,
FoucaudC.
1997; Nutritional requirements of Leuconostoc mesenteroides subsp.mesenteroides and subsp. dextranicum for growth in milk. J Dairy Res 64:95–103[CrossRef]
CharbonnelP.,
LamarqueM.,
PiardJ.-C.,
GilbertC.,
JuillardV.,
AtlanD.
2003; Diversity of oligopeptide transport specificity in Lactococcus lactis species. A tool to unravel the role of OppA in uptake specificity. J Biol Chem 278:14832–14840[CrossRef]
ChervauxC.,
EhrlichS. D.,
MaguinE.
2000; Physiological study of Lactobacillus delbrueckii subsp.bulgaricus strains in a novel chemically defined medium. Appl Environ Microbiol 66:5306–5311[CrossRef]
CourtinP.,
MonnetV.,
RulF.
2002; Cell-wall proteinase PrtS and PrtB have a different role in Streptococcus thermophilus/Lactobacillus bulgaricus mixed cultures in milk. Microbiology 148:3413–3421
DesmazeaudM. J.,
HermierJ. H.
1972; Isolement et détermination de la composition qualitative de peptides issus de la caséine, stimulant la croissance de Streptococcus thermophilus. Eur J Biochem 28:190–198[CrossRef]
DesmazeaudM. J.,
HermierJ. H.
1973; Effet de fragments peptidiques du glucagon vis-à-vis de la croissance de Streptococcus thermophilus. Biochimie 55:679–684[CrossRef]
DetmersF. J. M.,
KunjiE. R. S.,
LanfermeijerF. C.,
PoolmanB.,
KoningsW. N.
1998; Kinetics and specificity of peptide uptake by the oligopeptide transport system of Lactococcus lactis. Biochemistry 37:16671–16679[CrossRef]
DoevenM. K.,
AbeleR.,
PoolmanB, TampéR.2004; The binding specificity of OppA determines the selectivity of the oligopeptide ATP-binding cassette transporter. J Biol Chem 279:32301–32307[CrossRef]
EisenbergD.,
SchwartzE.,
KomaronyM.,
WallR.
1984; Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J Mol Biol 179:125–142[CrossRef]
GaraultP.,
LetortC.,
JuillardV.,
MonnetV.
2000; Branched-chain amino acid biosynthesis is essential for optimal growth of Streptococcus thermophilus in milk. Appl Environ Microbiol 66:5128–5133[CrossRef]
GaraultP.,
Le BarsD.,
BessetC.,
MonnetV.
2002; Three binding proteins are involved in the transport of oligopeptide by Streptococcus thermophilus. J Biol Chem 277:32–39[CrossRef]
HebertE. M.,
RayaR. R.,
De GioriG. S.
2000; Nutritional requirements and nitrogen-dependent regulation of proteinase activity of Lactobacillus helveticus CRL 1062. Appl Environ Microbiol 66:5316–5321[CrossRef]
HelinckS.,
CharbonnelP.,
PiardJ.-C.,
FoucaudC.,
JuillardV.
2003; Charged casein-derived oligopeptides competitively inhibit the transport of a reporter oligopeptide by Lactococcus lactis. J Appl Microbiol 94:900–907[CrossRef]
HerraizT.,
CasalV.,
PoloM. C.
1994; Reverse-phase HPLC analysis of peptides in standard and dairy samples using one-line absorbance and post-column OPA fluorescence detection. Z Lebensm Unters Forsch 199:265–269[CrossRef]
HugginsA. M.,
SandineW. E.
1984; Differentiation of fast and slow milk-coagulating isolates in strains of lactic streptococci. J Dairy Sci 67:1674–1679[CrossRef]
JenkinsonH. F.,
BakerR. A.,
TannockG. W.
1996; A binding-lipoprotein-dependent oligopeptide transport system in Streptococcus gordonii essential for uptake of hexa- and heptapeptides. J Bacteriol 178:68–77
JuillardV.,
Le BarsD.,
KunjiE. R. S.,
KoningsW. N.,
GriponJ.-C.,
RichardJ.
1995a; Oligopeptides are the main source of nitrogen for Lactococcus lactis during growth in milk. Appl Environ Microbiol 61:3024–3030
JuillardV.,
LaanH.,
KunjiE. R. S.,
Jeronimus-StratinghC. M.,
BruinsA. P.,
KoningsW. N.
1995b; The extracellular PI-type proteinase of Lactococcus lactis hydrolyses β-casein into more than one hundred different oligopeptides. J Bacteriol 177:3472–3478
KunjiE. R. S.,
HagtingA., de VriesC. J.,
JuillardV.,
HaandrickmanA.,
PoolmanB.,
KoningsW. N.
1995; Transport of β-casein derived peptides by the oligopeptide transport system is a crucial step in the proteolytic pathway ofLactococcus lactis
. J Biol Chem 270:1569–1574[CrossRef]
KunjiE. R. S.,
MierauI.,
HagtingA.,
PoolmanB.,
KoningsW. N.
1996; The proteolytic systems of lactic acid bacteria. Antonie Van Leeuwenhoek 70:187–221[CrossRef]
LamarqueM.,
CharbonnelP.,
AubelD.,
PiardJ.-C.,
AtlanD.,
JuillardV.
2004; A multifunction ABC transporter (Opt) contributes to diversity of peptide uptake specificity within the genus Lactococcus. J Bacteriol 186:6492–6500[CrossRef]
LanfermeijerF. C.,
PiconA.,
KoningsW. N.,
PoolmanB.
1999; Kinetics and consequences of binding of nona- and dodecapeptides to the oligopeptide binding protein (OppA) of Lactococcus lactis. Biochemistry 38:14440–14450[CrossRef]
LetortC.,
JuillardV.
2001; Development of a minimal chemically defined medium for the exponential growth of Streptococcus thermophilus. J Appl Microbiol 91:1023–1029[CrossRef]
LetortC.,
NardiM.,
GaraultP.,
CourtinP.,
MonnetV.,
JuillardV.
2002; Casein utilization by Streptococcus thermophilus results in a diauxic growth in milk. Appl Environ Microbiol 68:3162–3165[CrossRef]
LimauroD.,
FalciatoreA.,
BassoA. L.,
ForlaniG.,
De FeliceM.
1996; Proline biosynthesis in Streptococcus thermophilus: characterization of the proBA operon and its products. Microbiology 142:3275–3282[CrossRef]
MonnetV.,
Le BarsD.,
GriponJ.-C.
1987; Purification and characterization of a cell wall proteinase from Streptococcus lactis NCDO 763. J Dairy Res 54:247–255[CrossRef]
ShahbalS.,
HemmeD.,
RenaultP.
1993; Characterization of a cell envelope-associated proteinase activity from Streptococcus thermophilus H-strains. Appl Environ Microbiol 59:177–182
TameJ. R. H.,
MurshudovG. N.,
DodsonE. J.,
NeilT. K.,
DodsonG. G.,
HigginsC. F.,
WilkinsonA. J.
1994; The structural basis of sequence-independent peptide binding by OppA protein. Science 264:1578–1581[CrossRef]
TameJ. R. H.,
DodsonE. J.,
MurshudovG.,
HigginsC. F.,
WilkinsonA. J.
1995; The crystal structure of the oligopeptide-binding protein OppA complexed with tripeptide and tetrapeptide ligands. Structure 3:1395–1406[CrossRef]