Skip to main content
SpringerLink
Log in

2,5-Diketopiperazines Produced by Bacillus pumilus During Bacteriolysis of Arthrobacter citreus

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

We report the detection by gas chromatography/mass spectrometry and liquid chromatography/mass spectrometry analyses of the secreted 2,5-diketopiperazines (DKPs) cyclo(-Ala-Pro), cyclo(-Gly-Pro), cyclo(-Val-Pro), cyclo(-Ile-Pro), cyclo(-Leu-Pro), cyclo(-Pro-Pro), cyclo(-HyP-Pro), cyclo(-Met-Pro), and cyclo(-Phe-Pro) produced by Bacillus pumilus. The study focuses on a marine isolate and a laboratory test strain of B. pumilus with capabilities to lyse pregrown living cell lawns of different bacterial species, among them Arthrobacter citreus. Chromatographic methods were used to analyze induced bioactive compounds. At least 13 different DKPs are produced by B. pumilus. Both strains respond with an increased production of the DKPs cyclo(-Gly-Pro), cyclo(-Ala-Pro), and cyclo(-Val-Pro) to the presence of pasteurized A. citreus cells after 4 h in a nutrient-poor liquid medium. In agar diffusion assays, these DKPs did not cause lysis zones in living cell lawns, but they did inhibit further growth of several pregrown test bacteria in microplates even at concentrations as low as 1 μg ml−1. Antibiotic substances produced by B. pumilus after 20 h of cultivation in a special lysis medium showed lytic activity in cell-free extracts of B. pumilus culture supernatants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Berleman JE, Kirby JR (2009) Deciphering the hunting strategy of a bacterial wolfpack. FEMS Microbiol Rev 33:942–957

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bina XWR, Bina JE (2010) The cyclic dipeptide cyclo(Phe-Pro) inhibits cholera toxin and toxin-coregulated pilus production in O1 El Tor Vibrio cholerae. J Bacteriol 192:3829–3832

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brack C, Mikolasch A, Pukall R, Schumann P, Köster M, Schauer F (2013) Bacteriolytic Bacillus species isolated from brackish waters of the Southern Baltic Sea. Mar Biol 160(10):2699–2709

    Article  Google Scholar 

  • Burgess JG, Jordan EM, Bregu M, Mearns-Spragg A, Boyd KG (1999) Microbial antagonism: a neglected avenue of natural products research. J Biotechnol 70:27–32

    Article  CAS  PubMed  Google Scholar 

  • Chen MZ, Dewis ML, Kraut K, Merritt D, Reiber L, Trinnaman L, Da Costa NC (2009) 2,5-Diketopiperazines (cyclic dipeptides) in beef: identification, synthesis, and sensory evaluation. J Food Sci 74:C100–C105

    Article  CAS  PubMed  Google Scholar 

  • de Carvalho MP, Abraham WR (2012) Antimicrobial and biofilm inhibiting diketopiperazines. Curr Med Chem 19:3564–3577

    Article  PubMed  Google Scholar 

  • de Melo FMP, Fiore MF, de Moraes LAB, Silva-Stenico ME, Scramin S, Teixeira MD, de Melo IS (2009) Antifungal compound produced by the cassava endophyte Bacillus pumilus MAIIIM4a. Sci Agric 66:583–592

    Article  Google Scholar 

  • de Rosa S, Mitova M, Tommonaro G (2003) Marine bacteria associated with sponge as source of cyclic peptides. Biomol Eng 20:311–316

    Article  PubMed  Google Scholar 

  • Degrassi G, Aguilar C, Bosco M, Zahariev S, Pongor S, Venturi V (2002) Plant growth-promoting Pseudomonas putida WCS358 produces and secretes four cyclic dipeptides: cross-talk with quorum sensing bacterial sensors. Curr Microbiol 45:250–254

    Article  CAS  PubMed  Google Scholar 

  • Fiolka MJ, Witkowski A (2004) Lysozyme-like activity in eggs and in some tissues of land snails Helix aspersa maxima and Achatina achatina. Folia Biol-Krakow 52:233–237

    Article  CAS  PubMed  Google Scholar 

  • Fischer PM (2003) Diketopiperazines in peptide and combinatorial chemistry. J Pept Sci 9:9–35

    Article  CAS  PubMed  Google Scholar 

  • Folman LB, De Klein MJEM, Postma J, van Veen JA (2004) Production of antifungal compounds by Lysobacter enzymogenes isolate 3.1 T8 under different conditions in relation to its efficacy as a biocontrol agent of Pythium aphanidermatum in cucumber. Biol Control 31:145–154

    Article  CAS  Google Scholar 

  • Ginz M, Engelhardt UH (2001) Identification of new diketopiperazines in roasted coffee. Eur Food Res Technol 213:8–11

    Article  CAS  Google Scholar 

  • Grossart HP, Schlingloff A, Bernhard M, Simon M, Brinkhoff T (2004) Antagonistic activity of bacteria isolated from organic aggregates of the German Wadden Sea. FEMS Microbiol Ecol 47:387–396

    Article  CAS  PubMed  Google Scholar 

  • Gudasheva TA, Boyko SS, Akparov VK, Ostrovskaya RU, Skoldinov SP, Rozantsev GG, Voronina TA, Zherdev VP, Seredenin SB (1996) Identification of a novel endogenous memory facilitating cyclic dipeptide cyclo-prolylglycine in rat brain. FEBS Lett 391:149–152

    Article  CAS  PubMed  Google Scholar 

  • Holden MTG, Chhabra SR, de Nys R, Stead P, Bainton NJ, Hill PJ, Manefield M, Kumar N, Labatte M, England D, Rice S, Givskov M, Salmond GPC, Stewart GSAB, Bycroft BW, Kjelleberg SA, Williams P (1999) Quorum-sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other Gram-negative bacteria. Mol Microbiol 33:1254–1266

    Article  CAS  PubMed  Google Scholar 

  • Jurkevitch E, Davidov Y, Jurkevitch E (2007) Phylogenetic diversity and evolution of predatory prokaryotes, Predatory prokaryotes: biology, ecology and evolution. Springer, New York

    Book  Google Scholar 

  • Kumar N, Mohandas C, Nambisan B, Kumar DRS, Lankalapalli RS (2013) Isolation of proline-based cyclic dipeptides from Bacillus sp N strain associated with rhabitid entomopathogenic nematode and its antimicrobial properties. World J Microbiol Biotechnol 29:355–364

    Article  CAS  PubMed  Google Scholar 

  • Leisner JJ, Haaber J (2012) Intraguild predation provides a selection mechanism for bacterial antagonistic compounds. P Roy Soc Edinb B 279:4513–4521

    Article  CAS  Google Scholar 

  • Lu XL, Shen YH, Zhu YP, Xu QZ, Liu XY, Ni KY, Cao X, Zhang WD, Jiao BH (2009) Diketopiperazine constituents of marine Bacillus subtilis. Chem Nat Compd 45:290–292

    Article  CAS  Google Scholar 

  • Martin MO (2002) Predatory prokaryotes: an emerging research opportunity. J Mol Microbiol Biotechnol 4:467–477

    CAS  PubMed  Google Scholar 

  • Parisien A, Allain B, Zhang J, Mandeville R, Lan CQ (2008) Novel alternatives to antibiotics: bacteriophages, bacterial cell wall hydrolases, and antimicrobial peptides. J Appl Microbiol 104:1–13

    CAS  PubMed  Google Scholar 

  • Qi SH, Xu Y, Gao J, Qian PY, Zhang S (2009) Antibacterial and antilarval compounds from marine bacterium Pseudomonas rhizosphaerae. Ann Microbiol 59:229–233

    Google Scholar 

  • Rhee KH (2002) Isolation and characterization of Streptomyces sp KH-614 producing anti-VRE (vancomycin-resistant enterococci) antibiotics. J Gen Appl Microbiol 48:321–327

    Google Scholar 

  • Ryan LAM, Dal Bello F, Arendt EK, Koehler P (2009) Detection and quantitation of 2,5-diketopiperazines in wheat sourdough and bread. J Agric Food Chem 57:9563–9568

    Article  CAS  PubMed  Google Scholar 

  • Schauer F (1981). Untersuchungen zum Abbau von n-Dodecan durch Pseudomonas aeruginosa 7/4 II. Dissertation, Ernst–Moritz–Arndt–Universität Greifswald, Mathematisch-Naturwissenschaftliche-Fakultät

  • Seifert H, Merz D (2003) Primärseitige Stickoxidminderung als Beispiel für die Optimierung des Verbrennungsvorgangs in Abfallverbrennungsanlagen. Wissenschaftliche Berichte FZKA Karlsruhe. http://bibliothek.fzk.de/zb/berichte/FZKA6944.pdf. Accessed 1 Oct 2004

  • Trindade-Silva AE, Machado-Ferreira E, Senra MVX, Vizzoni VF, Yparraguirre LA, Leoncini O, Soares CAG (2009) Physiological traits of the symbiotic bacterium Teredinibacter turnerae isolated from the mangrove shipworm Neoteredo reynei. Genet Mol Biol 32:572–581

    Article  PubMed Central  PubMed  Google Scholar 

  • Trischman JA, Oeffner RE, Luna MGD, Kazaoka M (2004) Competitive induction and enhancement of indole and a diketopiperazine in marine bacteria. Mar Biotechnol 6:215–220

    Article  CAS  PubMed  Google Scholar 

  • Wang JH, Quan CS, Qi XH, Li X, Fan SD (2010) Determination of diketopiperazines of Burkholderia cepacia CF-66 by gas chromatography-mass spectrometry. Anal Bioanal Chem 396:1773–1779

    Article  CAS  PubMed  Google Scholar 

  • Xie YX, Wright S, Shen YM, Du LC (2012) Bioactive natural products from Lysobacter. Nat Prod Rep 29:1277–1287

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Anne Reinhard, Stefan Bock, and David Sengebusch for laboratory assistance; Bob Jack for reviewing the manuscript; Dr. Peter Schumann for the identification of Bacillus subtilis subspecies; and Prof. Dr. Lindequist and Prof. Dr. Riedel for providing the spectrometers. We also thank the government of Mecklenburg-Vorpommern (Germany) for financial support in the form of a Landesgraduiertenstipendium.

Author information

Authors and Affiliations

  1. Department of Applied Microbiology, Institute of Microbiology, University Greifswald, Friedrich-Ludwig-Jahn-Str. 15, 17487, Greifswald, Germany

    Christiane Brack, Annett Mikolasch & Frieder Schauer

Authors
  1. Christiane Brack
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Annett Mikolasch
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Frieder Schauer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christiane Brack.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 37.2 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Brack, C., Mikolasch, A. & Schauer, F. 2,5-Diketopiperazines Produced by Bacillus pumilus During Bacteriolysis of Arthrobacter citreus . Mar Biotechnol 16, 385–395 (2014). https://doi.org/10.1007/s10126-014-9559-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-014-9559-y

Keywords

Search

Navigation