Skip to main content

Advertisement

Log in

The effect of tryptophol on the bacteriophage infection in high-temperature environment

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Small metabolites can participate in the virus-host interactions in eukaryotes. However, little is known about roles of metabolites in the interactions between bacteria and bacteriophages. In this study, the metabolomic profilings of bacteriophage GVE2-infected and virus-free Geobacillus sp. E263, a thermophilic bacterium isolated from a deep-sea hydrothermal vent, were characterized. The results showed that metabolites tryptophol, adenine, and hydroxybenzylalcohol were significantly elevated in Geobacillus sp. E263 in response to the GVE2 infection. Furthermore, our data indicated that tryptophol was involved in the bacteriophage infection. Tryptophol could inhibit the infection/replication of GVE2 by interacting with the host’s Clp protease. Therefore, our study revealed novel aspects of metabolites during the bacteriophage infection in high-temperature environment.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adamski J, Suhre K (2012) Metabolomics platforms for genome wide association studies-linking the genome to the metabolome. Curr Opin Biotechnol 24:39–47

    Article  PubMed  Google Scholar 

  • Ankrah NYD, May AL, Middleton JL, Jones DR, Hadden MK, Gooding JR, LeCleir GR, Wilhelm SW, Campagna SR, Buchan A (2013) Phage infection of an environmentally relevant marine bacterium alters host metabolism and lysate composition. ISME J 8:1089–1100

    Article  PubMed Central  PubMed  Google Scholar 

  • Buchinger S, Strösser J, Rehm N, Hänßler E, Hans S, Bathe B, Schomburg D, Krämer R, Burkovski A (2009) A combination of metabolome and transcriptome analyses reveals new targets of the Corynebacterium glutamicum nitrogen regulator AmtR. J Biotechnol 140:68

  • Buckingham J (1998) Natural products Chemical nomenclature. Springer, Berlin, pp 162–207

  • Chen B, Dodge ME, Tang W, Lu J, Ma Z, Fan CW, Wei S, Hao W, Kilgore J, Williams NS, Roth MG, Amatruda JF, Chen C, Lum L (2009) Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat Chem Biol 5:100–107

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chen Y, Wei D, Wang Y, Zhang X (2013) The role of interactions between bacterial chaperone, aspartate aminotransferase, and viral protein during virus infection in high temperature environment: the interactions between bacterium and virus proteins. BMC Microbiol 13:48

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Erdoğan I, Şener B, Higa T (2000) Tryptophol, a plant auxin isolated from the marine sponge Ircinia spinulosa. Biochem Syst Ecol 28:793–794

    Article  Google Scholar 

  • Förster J, Famili I, Fu P, Palsson BØ, Nielsen J (2003) Genome-scale reconstruction of the Saccharomyces cerevisiae metabolic network. Genome Res 13:244–253

    Article  PubMed Central  PubMed  Google Scholar 

  • Fukusaki E, Kobayashi A (2005) Plant metabolomics: potential for practical operation. J Biosci Bioeng 100:347–354

    Article  CAS  PubMed  Google Scholar 

  • Garden SJ, da Silva RB, Pinto AC (2002) A versatile synthetic methodology for the synthesis of tryptophols. Tetrahedron 58:8399–8412

    Article  CAS  Google Scholar 

  • Grant M, Lamb C (2006) Systemic immunity. Curr Opin Plant Biol 9:414–420

    Article  CAS  PubMed  Google Scholar 

  • Inagaki S, Morimura S, Tang Y, Akutagawa H, Kida K (2007) Tryptophol induces death receptor (DR) 5-mediated apoptosis in U937 cells. Biosci Biotechnol Biochem 71:2065–2068

    Article  CAS  PubMed  Google Scholar 

  • Janelle M-E, Gravel A, Gosselin J, Tremblay MJ, Flamand L (2002) Activation of monocyte cyclooxygenase-2 gene expression by human herpesvirus 6 role for cylic AMP-responsive element-binding and activator protein-1. J Biol Chem 277:30665–30674

    Article  CAS  PubMed  Google Scholar 

  • Jin M, Ye T, Zhang X (2013) Roles of bacteriophage GVE2 endolysin in host lysis at high temperatures. Microbiology SGM 59:1597–1605

    Article  Google Scholar 

  • Jin M, Chen Y, Xu C, Zhang X (2014) The effect of inhibition of host MreB on the infection of thermophilic phage GVE2 in high temperature environment. Sci Rep 4:4823

    PubMed Central  PubMed  Google Scholar 

  • Khedkar V, Tillack A, Michalik M, Beller M (2005) Convenient synthesis of tryptophols and tryptophol homologues by hydroamination of alkynes. Tetrahedron 61:7622–7631

    Article  CAS  Google Scholar 

  • Knight V, Sanglier J-J, DiTullio D, Braccili S, Bonner P, Waters J, Hughes D, Zhang L (2003) Diversifying microbial natural products for drug discovery. Appl Microbiol Biotechnol 62:446–458

    Article  CAS  PubMed  Google Scholar 

  • Kutter E, Sulakvelidze A (2004) Bacteriophages: biology and applications. CRC Press, Boca Raton

    Book  Google Scholar 

  • Kutter E, Guttman B, Carlson K (1994) The transition from host to phage metabolism after T4 infection. In: Molecular Biology of Bacteriophage T4:343-346. American Society for Microbiology, Washington DC

  • Laachouch JE, Desmet L, Geuskens V, Grimaud R, Toussaint A (1996) Bacteriophage Mu repressor as a target for the Escherichia coli ATP-dependent Clp Protease. EMBO J 15:437

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lara-Pezzi E, Gómez-Gaviro MV, Gálvez BG, Mira E, Iñiguez MA, Fresno M, Martínez-A C, Arroyo AG, López-Cabrera M (2002) The hepatitis B virus X protein promotes tumor cell invasion by inducing membrane-type matrix metalloproteinase-1 and cyclooxygenase-2 expression. J Clin Invest 110:1831–1838

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li X, Gianoulis TA, Yip KY, Gerstein M, Snyder M (2010) Extensive in vivo metabolite-protein interactions revealed by large-scale systematic analyses. Cell 143:639–650

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lin S, Liu N, Yang Z, Song W, Wang P, Chen H, Lucio M, Schmitt-Kopplin P, Chen G, Cai Z (2010) GC/MS-based metabolomics reveals fatty acid biosynthesis and cholesterol metabolism in cell lines infected with influenza A virus. Talanta 83:262–268

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Wu S, Song Q, Zhang X, Xie L (2006) Two novel bacteriophages of thermophilic bacteria isolated from deep-sea hydrothermal fields. Curr Microbiol 53:163–166

    Article  CAS  PubMed  Google Scholar 

  • Loebenstein G (2009) Local lesions and induced resistance. Adv Virus Res 75:73–117

    Article  CAS  PubMed  Google Scholar 

  • Meyer H, Liebeke M, Lalk M (2010) A protocol for the investigation of the intracellular Staphylococcus aureus metabolome. Anal Biochem 401:250–259

    Article  CAS  PubMed  Google Scholar 

  • Mosig G, Eiserling F, Calendar R (2006) The bacteriophages. Oxford University Press, Oxford

    Google Scholar 

  • Moussatova A, Kandt C, O'Mara ML, Tieleman DP (2008) ATP-binding cassette transporters in Escherichia coli. Biochim Biophys Acta Biomembr 1778:1757–1771

    Article  CAS  Google Scholar 

  • Newman DJ, Cragg GM, Snader KM (2000) The influence of natural products upon drug discovery. Nat Prod Rep 17:215–234

    Article  CAS  PubMed  Google Scholar 

  • Paul AG, Chandran B, Sharma-Walia N (2013) Cyclooxygenase-2-prostaglandin E2-eicosanoid receptor inflammatory axis: a key player in Kaposi's sarcoma-associated herpes virus associated malignancies. Transl Res 162:77–92

    Article  CAS  PubMed  Google Scholar 

  • Peric-Concha N, Long PF (2003) Mining the microbial metabolome: a new frontier for natural product lead discovery. Drug Discov Today 8:1078–1084

    Article  CAS  PubMed  Google Scholar 

  • Poranen MM, Ravantti JJ, Grahn AM, Gupta R, Auvinen P, Bamford DH (2006) Global changes in cellular gene expression during bacteriophage PRD1 Infection. J Virol 80:8081–8088

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Porankiewicz J, Wang J, Clarke AK (1999) New insights into the ATP-dependent Clp protease: Escherichia coli and beyond. Mol Microbiol 32:449–458

  • Putri SP, Nakayama Y, Matsuda F, Uchikata T, Kobayashi S, Matsubara A, Fukusaki E (2013) Current metabolomics: practical applications. J Biosci Bioeng 115:579–589

    Article  CAS  PubMed  Google Scholar 

  • Ren W, Strobel G, Sears J, Park M (2010) Geobacillus sp., a thermophilic soil bacterium producing volatile antibiotics. Microb Ecol 60:130–136

    Article  CAS  PubMed  Google Scholar 

  • Roucourt B, Lavigne R (2009) The role of interactions between phage and bacterial proteins within the infected cell: a diverse and puzzling interactome. Environ Microbiol 11:2789–2805

    Article  CAS  PubMed  Google Scholar 

  • Schägger H (2006) Tricine-SDS-PAGE. Nat Protoc 1:16–22

    Article  PubMed  Google Scholar 

  • Srivastava S, Bisht H, Sidhu O, Srivastava A, Singh P, Pandey R, Raj S, Roy R, Nautiyal C (2012) Changes in the metabolome and histopathology of Amaranthus hypochondriacus L. in response to Ageratum enation virus infection. Phytochemistry 80:8–16

    Article  CAS  PubMed  Google Scholar 

  • Tomiyasu M, Aida N, Watanabe Y, Mori K, Endo K, Kusakiri K, Kershaw J, Obata T, Osaka H (2012) Monitoring the brain metabolites of children with acute encephalopathy caused by the H1N1 virus responsible for the 2009 influenza pandemic: a quantitative in vivo 1H MR spectroscopy study. Magn Reson Imaging 30:1527–1533

    Article  CAS  PubMed  Google Scholar 

  • Vincendeau P, Lesthelle S, Bertazzo A, Okomo-Assoumou M, Allegri G, Costa C (1999) Importance of L-tryptophan metabolism in trypanosomiasis. In: Tryptophan, serotonin, and melatonin. Springer, pp 525-531

  • Waris G, Siddiqui A (2005) Hepatitis C virus stimulates the expression of cyclooxygenase-2 via oxidative stress: role of prostaglandin E2 in RNA replication. J Virol 79:9725–9734

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wei D, Zhang X (2010) Proteomic analysis of interactions between a deep-sea thermophilic bacteriophage and its host at high temperature. J Virol 84:2365–2373

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wojtkowiak D, Georgopoulos C, Zylicz M (1993) Isolation and characterization of ClpX, a new ATP-dependent specificity component of the Clp protease of Escherichia coli. J Biol Chem 268:22609–22617

    CAS  PubMed  Google Scholar 

  • Yuan J, Doucette CD, Fowler WU, Feng X-J, Piazza M, Rabitz HA, Wingreen NS, Rabinowitz JD (2009) Metabolomics-driven quantitative analysis of ammonia assimilation in E coli. Mol Syst Biol 5:302

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by China Ocean Mineral Resources R & D Association (DY125-15-E-01), the National Natural Science Foundation of China (41276152), and Hi-Tech Research and Development Program of China (2012AA092103-5).

Conflict of interest

All the authors declared that they have no competing interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiaobo Zhang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jin, M., Xu, C. & Zhang, X. The effect of tryptophol on the bacteriophage infection in high-temperature environment. Appl Microbiol Biotechnol 99, 8101–8111 (2015). https://doi.org/10.1007/s00253-015-6674-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-015-6674-2

Keywords

Navigation