The second well-known system for peptide uptake is an ABC (ATP-binding cassette) transporter dedicated to oligopeptides (3 residues and more). Escherichia coli peptide binding protein OppA has a preference for positively charged peptides. 182, 25302535. A., Roux, E., Genay, M., Perrin, C., et al. Amino acid difference formula to help explain protein evolution. (2011). Specificity of milk peptide utilization by Lactococcus lactis. In this work, we aimed at investigating the peptide content of a commercial yeast extract (YE) and identifying dynamics of peptide utilization during the growth of the industrial S. thermophilus N4L strain, cultivated in 1 l bioreactors under pH-regulation. This work was funded by the Association Nationale de la Recherche et de la Technologie (ANRT, Contract Nr 2015/0599). (1995). LP and VJ wrote the manuscript. The boxes display the range between the first and third quartile of each distribution, and the central bold lines their median value. Ant. J. Biol. The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmicb.2019.00906/full#supplementary-material, Benjamini, Y., and Hochberg, Y. doi: 10.1128/jb.175.23.7523-7532.1993, Ummadi, M., and Curic-Bawden, M. (2008). The physicochemical class or barcode of the peptide is then defined as the combination of the respective intervals of the nine descriptors. doi: 10.1021/bi981712t, Detmers, F. J., Lanfermeijer, F. C., Abele, R., Jack, R. W., Tampe, R., Konings, W. N., et al. 71, 394406. Characteristics of the kinetic profiles. (2005). 279, 3230132307. However, as previously described, most of the identified peptides showed intermediate to low levels of spectral abundance (Table 3), which limits the relevance of a kinetic study directly at the single peptide scale. doi: 10.1016/j.jmb.2011.09.043, Kruskal, W. H., and Wallis, W. A. The cell-envelope located protease PrtS is the most plausible effector of this increase but the membrane-anchored protease HtrA could also play a role (Guillot et al., 2016). 76, 41934201. Opin. Anal. Biol. (2000). The positive charge was the result of both a higher and/or lower proportion of basic and acidic residues than other peptides, respectively. Table 5. The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. LP and EH performed the MS analyses. doi: 10.1007/978-94-017-2027-4_11, Colinge, J., Chiappe, D., Lagache, S., Moniatte, M., and Bougueleret, L. (2005). OppA and AmiA are lipoproteins anchored to the cell membrane and devoted to peptide binding and delivery to the translocon formed by OppBC/AmiCD. Finally, peptides enclosed in constant and fluctuating profiles displayed intermediate distributions regarding their length and net charge. Finally, spectral count data of remaining classes were modeled via a generalized linear model with a Poisson distribution. Three oligopeptide-binding proteins are involved in the oligopeptide transport of Streptococcus thermophilus. Reconstruction of the proteolytic pathway for use of beta-casein by Lactococcus lactis. In the case of DtpT, it has been evidenced in several species that it had a higher affinity for dipeptides over tripeptides, preferred hydrophobic substrates and worked less efficiently with cationic peptides (Nakajima et al., 1997; Fang et al., 2000; Solcan et al., 2012; Martinez Molledo et al., 2018). Both Opp and Ami share a similar overall genetic organization. (2017). The second axis mostly wore the information of the basic and aromatic content as well as peptide length. To estimate peptide relative abundance, spectral counting is considered as the simplest method in a label-free approach (Liu et al., 2004; Colinge et al., 2005). Each point represents a unique peptide. 
The limits of each interval chosen during the grouping were fixed according to the internal distribution of each physicochemical property established from the initial peptidome (t = 0 h) before inoculation (see Figure 2 for the representation of these intervals and the general rules regarding their constitution). Average number of peptides identified as a function of their relative abundance. Structural basis of substrate specificity in the serine proteases. Tynkkynen, S., Buist, G., Kunji, E., Kok, J., Poolman, B., Venema, G., et al. doi: 10.1074/jbc.M107002200, Goh, Y. J., Goin, C., OFlaherty, S., Altermann, E., and Hutkins, R. (2011). J. Bacteriol. The YE is composed of a large number of peptides displaying various physicochemical properties. Food Res. Charged casein-derived oligopeptides competitively inhibit the transport of a reporter oligopeptide by Lactococcus lactis. Microbiol. Each identified peptide was characterized by a combination of nine physicochemical properties. Biol. 29, 435463. The culture medium contained (w/v) 6% lactose, 0.01% calcium chloride and 2% of YE provided by Procelys (Maisons-Alfort, France) belonging to the Nucell range notably dedicated to dairy starters. Brew. These fragments can share the same barcodes as other peptides of the initial medium. (2012). Specialized adaptation of a lactic acid bacterium to the milk environment: the comparative genomics of Streptococcus thermophilus LMD-9. Controlling the false discovery rate: a practical and powerful approach to multiple testing. MassChroQ: a versatile tool for mass spectrometry quantification. Moreover, it has been formerly established in vivo that peptide transport in both species displayed very similar specificities (Juillard et al., 1998; Juille et al., 2005). (2016). 
Change-O: a toolkit for analyzing large-scale B cell immunoglobulin repertoire sequencing data. By pooling peptides into physicochemical classes, we were able (i) to identify consistent kinetic profiles, and (ii) to compensate partially for the overall low relative abundance levels of individual peptides. Peptide identification was performed with X!Tandem version 2015.12.15.2 (Vengeance) and X!TandemPipeline (C++) version 0.2.16 (Langella et al., 2016) on the protein sequence of Saccharomyces cerevisiae S288C (version 2015-01-13)1. 8:2285. doi: 10.3389/fmicb.2017.02285, Pasupuleti, V. K., and Braun, S. (2008). J. Biol. A simple method for displaying the hydropathic character of a protein. A linear gradient of acetonitrile (1.6% per min) in ammonium formate (20 mM, pH 6.2) was applied with a 0.7 ml per min flow rate and fractions were collected every minute. vannamei digestibility litopenaeus yeast extract utilization Briefly, the activated cartridge was loaded with 4 ml of sample, washed with 5% ACN and 0.1% TFA, and peptides were finally eluted with 1.5 ml of 50% ACN and 0.1% TFA in MilliQ water (Waters, St-Quentin-en-Yvelines, France). Membrane topology of the di- and tripeptide transport protein of Lactococcus lactis. (2011). 122, 110115. Preliminary analyses showed that the initial and last fractions collected, respectively, before 5 min and after 25 min of the chromatographic run contained less than 5% of the identified peptides (data not shown) and thus were discarded. An exclusion window of 40 s was applied. Then, a second filter was used on the 268 remaining abundant classes in order to remove those considered largely constant, i.e., showing less than 50% of variation between their minimal and maximal abundance values in the different samples. Table 4. Our work, by relying on a vastly higher number of peptides, not only consolidates these former results but also suggests a dominant role of a positive net charge for peptide transport. Am. (2016). A. J. Proteome Res. This transport was mediated by the Ami system which is the only oligopeptide carrier identified in the strain. Multispecific substrate recognition in a proton-dependent oligopeptide transporter. A kinetic profiling was then manually performed in order to separate classes showing either a decrease, increase or fluctuating variations over-time. Bioinformatics 31, 33563358. The number of identified peptides was large enough with an appropriate physicochemical diversity to enable a robust analysis of peptide utilization by S. thermophilus N4L. J. Transport of beta-casein-derived peptides by the oligopeptide transport system is a crucial step in the proteolytic pathway of Lactococcus lactis. S. thermophilus N4L was cultivated in a YE-based medium in 1 l bioreactors. doi: 10.1021/ac0498563, Mann, H. B., and Whitney, D. R. (1947). We thank the INRA PAPPSO proteomics platform (http://pappso.inra.fr supported by the Ile-de-France regional council and IBISA) for providing mass spectrometry facilities. They are thus mainly employed as amino nitrogen sources. yeast grisp soluble dehydrated doi: 10.1002/jib.298, Klepsch, M. M., Kovermann, M., Lw, C., Balbach, J., Permentier, H. P., Fusetti, F., et al. 10:906. doi: 10.3389/fmicb.2019.00906. FEMS Microbiol. B., Rios-Solis, L., and Halim, M. (2017). J. Biol. Hagting, A., Kunji, E. R., Leenhouts, K. J., Poolman, B., and Konings, W. N. (1994). 57, 640649. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). 105, 511522. All the modus operandi of the second chromatographic separation and peptide m/z detection were the same as those previously described (Guillot et al., 2016). doi: 10.1016/j.foodres.2016.04.039, Jpelt, K. B., Johnsen, L. G., and Christensen, J. H. (2016). Classes showing low abundance (<5 spectra in all samples) and little variations (less than 50% of variation between the minimal and maximal average abundance observed in the different samples) were discarded. Table 3. Educ. These profiles were classified into 3 different groups: classes showing an unambiguous decrease (36 classes) or increase (2 classes) over time, and classes whose time-course evolution was fluctuating (11 classes). Terzaghi, B. E., and Sandine, W. E. (1975). A contingency table was generated beforehand that contained the total spectral counts of each physicochemical class i.e., the sum of the spectral counts of their constitutive peptides in each analyzed sample. It is thus reasonable to assume that most, if not all, of these decreasing peptides were actually preferentially consumed by the strain and transported inside the cells. (2004). Oleic acid and related compounds as growth factors for lactic acid bacteria. Prog. 408,23032307. 4, 337360. All authors contributed to conception and design of the study, to manuscript revision, and approved the submitted version. Their kinetic profiles are depicted in Supplementary Figure S3. (1993). Peptide ionization was performed with a spray voltage of 1.3 kV. Therefore, DtpT and Ami are the only known peptide transport systems identified in this strain. Digestomics: an emerging strategy for comprehensive analysis of protein catabolism. Peptide ions were analyzed by the data-dependent method as follows: full MS scan (m/z 3501,600) was performed on the Orbitrap mass analyzer and the six most abundant doubly and triply charged peptides were submitted to MS/MS analysis with a collision energy of 35%. 25, 118. 233, 129142. This hypothesis is supported by the fact that increasing classes are constituted of numerous scarce peptides, many of which were only detected in the latter stages of fermentation. Indeed, the only known LAB peptidases able to convert peptides into free amino acids are intracellularly located (Christensen et al., 1999; Savijoki et al., 2006). They are summarized in Table 1. The internal distributions of each property calculated from the initial medium peptidome (before inoculation, t = 0 h) are represented in Figure 2. 21, 170201. doi: 10.2307/3001968. doi: 10.1002/btpr.2110. These two combined systems, DtpT and Opp/Ami, allow for a large supply of various peptides to the bacterial cells. (1997). 175, 75237532. doi: 10.1073/pnas.220308797, Doeven, M. K., Abele, R., Tamp, R., and Poolman, B. Bioanal. doi: 10.1007/978-4-431-54607-8_20, Jameh, N., Galia, W., Awussi, A. 28, 13321340. It therefore indicates that the specificity of casein cleavage by PrtS will determine the capability of released peptides to be used by S. thermophilus during growth in milk. doi: 10.1007/s10482-013-0103-2, Kevvai, K., Ktt, M.-L., Nisamedtinov, I., and Paalme, T. (2016). The characterization of amino acid sequences in proteins by statistical methods. Front. doi: 10.1111/j.2517-6161.1995.tb02031.x, Berntsson, R. P., Thunnissen, A. M., Poolman, B., and Slotboom, D.-J. 
doi: 10.1007/978-1-4020-6674-0_2, Perona, J. J., and Craik, C. S. (1995). These patterns might come from two plausible origins: transport inside the cells, and/or peptide cleavage mediated by an extracellular hydrolytic activity. J. Proteome Res. This finding was subsequently found to apply as well to S. typhimurium OppA. Microbiol. Peptide identification was performed on the initial medium before inoculation (t = 0 h) and then each hour from 3 to 6 h of growth, corresponding to the exponential and the early stationary growth phases (Supplementary Figure S1). Peptidases and amino acid catabolism in lactic acid bacteria. doi: 10.1016/j.jbiotec.2016.04.031, Spearman, M., Lodewyks, C., Richmond, M., and Butler, M. (2014). Similarly, the consumption of positively charged peptides by S. thermophilus N4L is likely to be essentially dictated by its own oligopeptide-binding proteins, namely AmiA1 and AmiA3. Chem. Diversity of oligopeptide transport specificity in Lactococcus lactis species. Microb. Two successive precultures were performed prior to inoculating at 2% (v/v) the fermenters. The bioactivity and fractionation of peptide hydrolysates in cultures of CHO cells. Genetic and biochemical characterization of the oligopeptide transport system of Lactococcus lactis. 7:e01029-18. This confirms that non-tryptic peptide identification in complex mixtures is still technically challenging, as already discussed (Guillot et al., 2016). On the other hand, peptide utilization is also dependent on the transport machinery of the cultivated LAB. The physicochemical properties of peptides belonging to the different kinetic profiles were then discriminated by a principal component analysis (PCA) (R package FactoMineR version 1.41, L et al., 2008). Most of the nine physicochemical properties of the peptides initially identified were distributed within a relatively broad range, reflecting a large physicochemical diversity. doi: 10.1016/0022-2836(82)90515-0, Lanfermeijer, F. C., Detmers, F. J., Konings, W. N., and Poolman, B. MP was employed by Sacco S.r.l. Copyright 2019 Proust, Sourabi, Pedersen, Besanon, Haudebourg, Monnet and Juillard. Concerning the oligopeptide carrier specificity, extensive information is available about L. lactis Opp. doi: 10.1126/science.185.4154.862, Guillot, A., Boulay, M., Chambellon,, Gitton, C., Monnet, V., and Juillard, V. (2016). J. Stat. 193, 42544256. The three repetitions are represented separately. Development of a minimal chemically-defined medium for the exponential growth of Streptococcus thermophilus. Ant. Finally, we also thank Simon Poirier, Rozenn Gardan and Franoise Rul for their critical reading and helpful discussions. In order of importance, the first axis separated the peptides according to their polarity, acidic content, charge, hydrophobicity and, to a lesser extent, peptide bulkiness. Fractionation of yeast extract by nanofiltration process to assess key compounds involved in CHO cell culture improvement. 269, 1139111399. In order to maximize reproducibility, samples from the two subsequent repetitions were taken when the added volumes of base reached the corresponding levels of the first repetition. On the binding mechanism of the peptide receptor of the oligopeptide transport system of Lactococcus lactis. The underlying idea was to pool peptides showing close physicochemical properties into groups in order to combine their spectral counts and therefore perform the study not with individual peptides but on a larger scale (see section Materials and Methods section for explanations about the grouping procedure). Nevertheless, the qualitative identification of peptides was not as effective, as, for a given time, only an average of 55% of the peptides was identified in all three repetitions. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Protein Sci. The main source of amino acids during growth of S. thermophilus in milk are caseins. Lactic acid bacteria (LAB) are a group of microorganisms displaying a wide range of properties making them suitable for various applications in fields such as health (Hill et al., 2017), chemistry (Othman et al., 2017; Sauer et al., 2017), or cosmetics (Izawa and Sone, 2014). The efficient clade: lactic acid bacteria for industrial chemical production. Thus, they are likely to be the most abundant in the medium. Appl. The editor and reviewer's affiliations are the latest provided on their Loop research profiles and may not reflect their situation at the time of review. Use of ranks in one-criterion variance analysis. Biochemistry 37, 1667116679. Physicochemical properties of the peptides initially present in YE before inoculation (t = 0 h). Stat. Chem. For that purpose, a specific procedure was performed in order to assign every identified peptide to a unique physicochemical class. 8):99. doi: 10.1186/1753-6561-5-S8-P99, Mosser, M., Kapel, R., Chevalot, I., Olmos, E., Marc, I., Marc, A., et al. 1):S22. In contrast, increasing profile was made up of exclusively negatively charged peptides that were also significantly longer (median length of 11 amino acids) and contained a higher amount of proline (median content = 18%). The main peptide identification parameters were the following: no cleavage specificity, variable methionine oxidation state and mass tolerance for parent and fragment ions of 10 ppm and 0.4 Da, respectively. J. Inst. In conclusion, the identification of complex mixtures of peptides by mass spectrometry, although still technically challenging, is progressively gaining attention (Bingeman et al., 2017) and is proving to be an excellent exploratory approach to unravel the peptide content of complex media but also to study the diverse oligopeptide utilization patterns of a bacterial species during its growth. Theoretically, there are 39 = 19,683 different possible classes or barcodes. Practically, not all are physically possible or exist biologically, and experimentally only 1,308 were identified here. doi: 10.1016/j.femsre.2005.04.008, Izawa, N., and Sone, T. (2014). Soc. doi: 10.18637/jss.v025.i01, Letort, C., and Juillard, V. (2001). Even though label-free mass spectrometry only allows relative quantification, these peptides are likely to be either the less abundant ones, or to have poor yields of detection. doi: 10.1016/j.copbio.2016.11.004, Charbonnel, P., Lamarque, M., Piard, J.-C., Gilbert, C., Juillard, V., and Atlan, D. (2003). doi: 10.1186/1475-2859-10-S1-S22, Grantham, R. (1974). A pool of vitamins as used in S. thermophilus chemically defined medium (Letort and Juillard, 2001) was also added in the culture medium in order to ensure repeatable and optimal growth performances similar to those obtained with equivalent Tween 80-containing media (data not shown). No use, distribution or reproduction is permitted which does not comply with these terms. Appl. doi: 10.1021/acs.jproteome.6b00632, L, S., Josse, J., and Husson, F. (2008). Microbiol. The proteolytic systems of lactic acid bacteria. A first filter was applied to remove all classes showing low levels of abundance (less than 5 spectra per class) as their quantification over time would not be relevant. 15.4 2 (Zimmerman et al., 1968). Cosmetic ingredients fermented by lactic acid bacteria, in Microbial Production, eds H. Anazawa and S. Shimizu (Tokyo: Springer), 233242. Leeuwen. This last finding suggests a slight over-representation in the yeast-derived peptide sequences of relatively small residues. 5(Suppl. Ann. It has also been found in S. thermophilus where it has been named Ami due to its high sequence homology with other streptococcal transporters (Garault et al., 2002). Appl. The generated p-values were adjusted by a FDR procedure (Benjamini and Hochberg, 1995). Moreover, these peptides were less polar, and they also contained a higher proportion of hydrophobic residues.
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