1887

Abstract

Oligopeptide-permeases (Opps) are used by bacteria to import short peptides. In addition to their metabolic benefit, imported short peptides are used in many Gram-positive bacteria as signalling molecules of the RRNPP super-family of quorum-sensing systems, making Opps an integral part of cell–cell communication. In some Gram-positive bacteria there exist multiple Opps and the relative importance of those to RRNPP quorum sensing are not fully clear. Specifically, in , the Gram-positive model species, there exist two homologous oligopeptide permeases named Opp and App. Previous work showed that the App system is mutated in lab strain 168 and its recovery partially complements an Opp mutation for several developmental processes. Yet, the nature of the impact of App on signalling and development in wild-type strains, where both permeases are active was not studied. Here we re-examine the impact of the two permease systems. We find that App has a minor contribution to biofilm formation, surfactin production and phage infection compared to the effect of Opp. This reduced effect is also reflected in its lower ability to import the signals of four different Rap-Phr RRNPP systems. Further analysis of the App system revealed that, unlike Opp, some App genes have undergone horizontal transfer, resulting in two distinct divergent alleles of this system in strains. We found that both alleles were substantially better adapted than the Opp system to import an exogenous RRNPP signal of the group PlcR-PapR system. In summary, we find that the App system has only a minor role in signalling but may still be crucial for the import of other peptides.

Funding
This study was supported by the:
  • HORIZON EUROPE European Research Council (Award 724805)
    • Principle Award Recipient: AvigdorEldar
  • Israel Science Foundation (Award 2288/2021)
    • Principle Award Recipient: AvigdorEldar
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001382
2023-09-27
2024-05-04
Loading full text...

Full text loading...

/deliver/fulltext/micro/169/9/mic001382.html?itemId=/content/journal/micro/10.1099/mic.0.001382&mimeType=html&fmt=ahah

References

  1. Monnet V. Bacterial oligopeptide-binding proteins. Cell Mol Life Sci 2003; 60:2100–2114 [View Article] [PubMed]
    [Google Scholar]
  2. Koide A, Hoch JA. Identification of a second oligopeptide transport system in Bacillus subtilis and determination of its role in sporulation. Mol Microbiol 1994; 13:417–426 [View Article] [PubMed]
    [Google Scholar]
  3. Harwood CR, Kikuchi Y. The ins and outs of Bacillus proteases: activities, functions and commercial significance. FEMS Microbiol Rev 2021; 46:fuab046 [View Article] [PubMed]
    [Google Scholar]
  4. Slamti L, Lereclus D. The oligopeptide ABC-importers are essential communication channels in gram-positive bacteria. Res Microbiol 2019; 170:338–344 [View Article] [PubMed]
    [Google Scholar]
  5. Garault P, Le Bars D, Besset C, Monnet V. Three oligopeptide-binding proteins are involved in the oligopeptide transport of Streptococcus thermophilus. J Biol Chem 2002; 277:32–39 [View Article] [PubMed]
    [Google Scholar]
  6. Rocha-Estrada J, Aceves-Diez AE, Guarneros G, de la Torre M. The RNPP family of quorum-sensing proteins in gram-positive bacteria. Appl Microbiol Biotechnol 2010; 87:913–923 [View Article] [PubMed]
    [Google Scholar]
  7. Aframian N, Eldar A. A bacterial tower of babel: quorum-sensing signaling diversity and its evolution. Annu Rev Microbiol 2020; 74:587–606 [View Article] [PubMed]
    [Google Scholar]
  8. Neiditch MB, Capodagli GC, Prehna G, Federle MJ. Genetic and structural analyses of RRNPP intercellular peptide signaling of gram-positive bacteria. Annu Rev Genet 2017; 51:311–333 [View Article] [PubMed]
    [Google Scholar]
  9. Even-Tov E, Omer Bendori S, Pollak S, Eldar A. Transient duplication-dependent divergence and horizontal transfer underlie the evolutionary dynamics of bacterial cell-cell signaling. PLoS Biol 2016; 14:e2000330 [View Article] [PubMed]
    [Google Scholar]
  10. Breuer RJ, Hirt H, Dunny GM. Mechanistic features of the Enterococcal pCF10 sex pheromone response and the biology of Enterococcus faecalis in its natural habitat. J Bacteriol 2018; 200:e00733-17 [View Article] [PubMed]
    [Google Scholar]
  11. Singh PK, Ramachandran G, Ramos-Ruiz R, Peiró-Pastor R, Abia D et al. Mobility of the native Bacillus subtilis conjugative plasmid pLS20 is regulated by intercellular signaling. PLoS Genet 2013; 9:e1003892 [View Article] [PubMed]
    [Google Scholar]
  12. Johnson CM, Grossman AD. Integrative and Conjugative Elements (ICEs): what they do and how they work. Annu Rev Genet 2015; 49:577–601 [View Article] [PubMed]
    [Google Scholar]
  13. Fontaine L, Boutry C, de Frahan MH, Delplace B, Fremaux C et al. A novel pheromone quorum-sensing system controls the development of natural competence in Streptococcus thermophilus and Streptococcus salivarius. J Bacteriol 2010; 192:1444–1454 [View Article] [PubMed]
    [Google Scholar]
  14. Rudner DZ, LeDeaux JR, Ireton K, Grossman AD. The spo0K locus of Bacillus subtilis is homologous to the oligopeptide permease locus and is required for sporulation and competence. J Bacteriol 1991; 173:1388–1398 [View Article] [PubMed]
    [Google Scholar]
  15. Gohar M, Faegri K, Perchat S, Ravnum S, Økstad OA et al. The PlcR virulence regulon of Bacillus cereus. PLoS One 2008; 3:1–9 [View Article] [PubMed]
    [Google Scholar]
  16. Perchat S, Talagas A, Poncet S, Lazar N, Li de la Sierra-Gallay I et al. How quorum sensing connects sporulation to necrotrophism in Bacillus thuringiensis. PLoS Pathog 2016; 12:e1005779 [View Article] [PubMed]
    [Google Scholar]
  17. Erez Z, Steinberger-Levy I, Shamir M, Doron S, Stokar-Avihail A et al. Communication between viruses guides lysis-lysogeny decisions. Nature 2017; 541:488–493 [View Article] [PubMed]
    [Google Scholar]
  18. Cosby WM, Vollenbroich D, Lee OH, Zuber P. Altered srf expression in Bacillus subtilis resulting from changes in culture pH is dependent on the Spo0K oligopeptide permease and the ComQX system of extracellular control. J Bacteriol 1998; 180:1438–1445 [View Article] [PubMed]
    [Google Scholar]
  19. Perego M, Higgins CF, Pearce SR, Gallagher MP, Hoch JA. The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol Microbiol 1991; 5:173–185 [View Article] [PubMed]
    [Google Scholar]
  20. Roggiani M, Dubnau D. ComA, a phosphorylated response regulator protein of Bacillus subtilis, binds to the promoter region of srfA. J Bacteriol 1993; 175:3182–3187 [View Article] [PubMed]
    [Google Scholar]
  21. Hoch JA. Regulation of the phosphorelay and the initiation of sporulation in Bacillus subtilis. Annu Rev Microbiol 1993; 47:441–465 [View Article] [PubMed]
    [Google Scholar]
  22. Aframian N, Omer Bendori S, Kabel S, Guler P, Stokar-Avihail A et al. Dormant phages communicate via arbitrium to control exit from lysogeny. Nat Microbiol 2022; 7:145–153 [View Article] [PubMed]
    [Google Scholar]
  23. Levdikov VM, Blagova EV, Brannigan JA, Wright L, Vagin AA et al. The structure of the oligopeptide-binding protein, AppA, from Bacillus subtilis in complex with a nonapeptide. J Mol Biol 2005; 345:879–892 [View Article] [PubMed]
    [Google Scholar]
  24. Hughes AM, Darby JF, Dodson EJ, Wilson SJ, Turkenburg JP et al. Peptide transport in Bacillus subtilis - structure and specificity in the extracellular solute binding proteins OppA and DppE. Microbiology 2022; 168: [View Article] [PubMed]
    [Google Scholar]
  25. McLoon AL, Guttenplan SB, Kearns DB, Kolter R, Losick R. Tracing the domestication of a biofilm-forming bacterium. J Bacteriol 2011; 193:2027–2034 [View Article] [PubMed]
    [Google Scholar]
  26. Stanley NR, Lazazzera BA. Defining the genetic differences between wild and domestic strains of Bacillus subtilis that affect poly-gamma-dl-glutamic acid production and biofilm formation. Mol Microbiol 2005; 57:1143–1158 [View Article] [PubMed]
    [Google Scholar]
  27. Kearns DB, Losick R. Swarming motility in undomesticated Bacillus subtilis. Mol Microbiol 2003; 49:581–590 [View Article] [PubMed]
    [Google Scholar]
  28. Dubois T, Lemy C, Perchat S, Lereclus D. The signaling peptide NprX controlling sporulation and necrotrophism is imported into Bacillus thuringiensis by two oligopeptide permease systems. Mol Microbiol 2019; 112:219–232 [View Article] [PubMed]
    [Google Scholar]
  29. Anagnostopoulos C, Spizizen J. Requirement for transformation in Bacillus subtilis. J Bacteriol 1961; 81:741–746 [View Article] [PubMed]
    [Google Scholar]
  30. Harwood C, Cutting SM. Molecular Biological Methods for Bacillus Chichester, New York: Wiley; 1990
    [Google Scholar]
  31. Omer Bendori S, Pollak S, Hizi D, Eldar A. The RapP-PhrP quorum-sensing system of Bacillus subtilis strain NCIB3610 affects biofilm formation through multiple targets, due to an atypical signal-insensitive allele of RapP. J Bacteriol 2015; 197:592–602 [View Article] [PubMed]
    [Google Scholar]
  32. Branda SS, González-Pastor JE, Ben-Yehuda S, Losick R, Kolter R. Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci 2001; 98:11621–11626 [View Article] [PubMed]
    [Google Scholar]
  33. Wach A. PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cerevisiae. Yeast 1996; 12:259–265 [View Article] [PubMed]
    [Google Scholar]
  34. Koo B-M, Kritikos G, Farelli JD, Todor H, Tong K et al. Construction and analysis of two genome-scale deletion libraries for Bacillus subtilis. Cell Syst 2017; 4:291–305 [View Article] [PubMed]
    [Google Scholar]
  35. Konkol MA, Blair KM, Kearns DB. Plasmid-encoded ComI inhibits competence in the ancestral 3610 strain of Bacillus subtilis. J Bacteriol 2013; 195:4085–4093 [View Article] [PubMed]
    [Google Scholar]
  36. Hamon MA, Lazazzera BA. The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol Microbiol 2001; 42:1199–1209 [View Article] [PubMed]
    [Google Scholar]
  37. Auchtung JM, Lee CA, Grossman AD. Modulation of the ComA-dependent quorum response in Bacillus subtilis by multiple Rap proteins and Phr peptides. J Bacteriol 2006; 188:5273–5285 [View Article] [PubMed]
    [Google Scholar]
  38. Bareia T, Pollak S, Eldar A. Self-sensing in Bacillus subtilis quorum-sensing systems. Nat Microbiol 2018; 3:83–89 [View Article] [PubMed]
    [Google Scholar]
  39. van Gestel J, Bareia T, Tenennbaum B, Dal Co A, Guler P et al. Short-range quorum sensing controls horizontal gene transfer at micron scale in bacterial communities. Nat Commun 2021; 12:2324 [View Article] [PubMed]
    [Google Scholar]
  40. Babel H, Naranjo-Meneses P, Trauth S, Schulmeister S, Malengo G et al. Ratiometric population sensing by a pump-probe signaling system in Bacillus subtilis. Nat Commun 2020; 11:1176 [View Article] [PubMed]
    [Google Scholar]
  41. Pottathil M, Lazazzera BA. The extracellular Phr peptide-Rap phosphatase signaling circuit of Bacillus subtilis. Front Biosci 2003; 8:d32–d45 [View Article] [PubMed]
    [Google Scholar]
  42. Zhu B, Stülke J. SubtiWiki in 2018: from genes and proteins to functional network annotation of the model organism Bacillus subtilis. Nucleic Acids Res 2018; 46:D743–D748 [View Article] [PubMed]
    [Google Scholar]
  43. Nicolas P, Mäder U, Dervyn E, Rochat T, Leduc A et al. Condition-dependent transcriptome reveals high-level regulatory architecture in Bacillus subtilis. Science 2012; 335:1103–1106 [View Article] [PubMed]
    [Google Scholar]
  44. Koide A, Perego M, Hoch JA. ScoC regulates peptide transport and sporulation initiation in Bacillus subtilis. J Bacteriol 1999; 181:4114–4117 [View Article] [PubMed]
    [Google Scholar]
  45. Soria-Carrasco V, Talavera G, Igea J, Castresana J. The K tree score: quantification of differences in the relative branch length and topology of phylogenetic trees. Bioinformatics 2007; 23:2954–2956 [View Article] [PubMed]
    [Google Scholar]
  46. Gominet M, Slamti L, Gilois N, Rose M, Lereclus D. Oligopeptide permease is required for expression of the Bacillus thuringiensis plcR regulon and for virulence. Mol Microbiol 2001; 40:963–975 [View Article] [PubMed]
    [Google Scholar]
  47. Slamti L, Lereclus D. A cell-cell signaling peptide activates the PlcR virulence regulon in bacteria of the Bacillus cereus group. EMBO J 2002; 21:4550–4559 [View Article] [PubMed]
    [Google Scholar]
  48. Lereclus D, Agaisse H, Gominet M, Salamitou S, Sanchis V. Identification of a Bacillus thuringiensis gene that positively regulates transcription of the phosphatidylinositol-specific phospholipase C gene at the onset of the stationary phase. J Bacteriol 1996; 178:2749–2756 [View Article] [PubMed]
    [Google Scholar]
  49. Mueller JP, Bukusoglu G, Sonenshein AL. Transcriptional regulation of Bacillus subtilis glucose starvation-inducible genes: control of gsiA by the ComP-ComA signal transduction system. J Bacteriol 1992; 174:4361–4373 [View Article] [PubMed]
    [Google Scholar]
  50. Picon A, van Wely KHM. Peptide binding to the Bacillus Subtilis oligopeptide-binding proteins OppA and AppA. Mol Biol Today 2001; 2:21–25
    [Google Scholar]
  51. Yoshida K, Yamaguchi H, Kinehara M, Ohki Y, Nakaura Y et al. Identification of additional TnrA-regulated genes of Bacillus subtilis associated with a TnrA box. Mol Microbiol 2003; 49:157–165 [View Article] [PubMed]
    [Google Scholar]
  52. Zaprasis A, Brill J, Thüring M, Wünsche G, Heun M et al. Osmoprotection of Bacillus subtilis through import and proteolysis of proline-containing peptides. Appl Environ Microbiol 2013; 79:576–587 [View Article] [PubMed]
    [Google Scholar]
  53. Solomon J, Su L, Shyn S, Grossman AD. Isolation and characterization of mutants of the Bacillus subtilis oligopeptide permease with altered specificity of oligopeptide transport. J Bacteriol 2003; 185:6425–6433 [View Article] [PubMed]
    [Google Scholar]
  54. Berntsson R-A, Schuurman-Wolters GK, Dunny G, Slotboom D-J, Poolman B. Structure and mode of peptide binding of pheromone receptor PrgZ. J Biol Chem 2012; 287:37165–37170 [View Article] [PubMed]
    [Google Scholar]
  55. Pollak S, Omer-Bendori S, Even-Tov E, Lipsman V, Bareia T et al. Facultative cheating supports the coexistence of diverse quorum-sensing alleles. Proc Natl Acad Sci 2016; 113:2152–2157 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001382
Loading
/content/journal/micro/10.1099/mic.0.001382
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error