Isolation, genomic and metabolomic characterization of Streptomyces tendae VITAKN with quorum sensing inhibitory activity from Southern India

Nabila Mohammed Ishaque; Ilia Burgsdorf; Jessie James Limlingan Malit; Subhasish Saha; Roberta Teta; Daniela Ewe; Krishnan Kannabiran; Pavel Hrouzek; Laura Steindler; Valeria Costantino; Kumar Saurav

doi:10.3390/microorganisms8010121

Isolation, genomic and metabolomic characterization of Streptomyces tendae VITAKN with quorum sensing inhibitory activity from Southern India

Nabila Mohammed Ishaque, Ilia Burgsdorf, Jessie James Limlingan Malit, Subhasish Saha, Roberta Teta, Daniela Ewe, Krishnan Kannabiran, Pavel Hrouzek, Laura Steindler, Valeria Costantino, Kumar Saurav

Department of Marine Biology

Research output: Contribution to journal › Article › peer-review

Abstract

Streptomyces are among the most promising genera in terms of production ability to biosynthesize a variety of bioactive secondary metabolites with pharmaceutical interest. Coinciding with the increase in genomic sequencing of these bacteria, mining of their genomes for biosynthetic gene clusters (BGCs) has become a routine component of natural product discovery. Herein, we describe the isolation and characterization of a Streptomyces tendae VITAKN with quorum sensing inhibitory (QSI) activity that was isolated from southern coastal part of India. The nearly complete genome consists of 8,621,231bp with a GC content of 72.2%. Sequence similarity networks of the BGCs detected from this strain against the Minimum Information about a Biosynthetic Gene Cluster (MIBiG) database and 3365 BGCs predicted by antiSMASH analysis of publicly available complete Streptomyces genomes were generated through the BiG-SCAPE-CORASON platform to evaluate its biosynthetic novelty. Crude extract analysis using high-performance liquid chromatography connected to high resolution tandem mass spectrometry (HPLC-HRMS/MS) and dereplication through the Global Natural Product Social Molecular Networking (GNPS) online workflow resulted in the identification of cyclic dipeptides (2, 5-diketopiperazines, DKPs) in the extract, which are known to possess QSI activity. Our results highlight the potential of genome mining coupled with LC-HRMS/MS and in silico tools (GNPS) as a valid approach for the discovery of novel QSI lead compounds. This study also provides the biosynthetic diversity of BGCs and an assessment of the predicted chemical space yet to be discovered.

Original language	English
Article number	121
Journal	Microorganisms
Volume	8
Issue number	1
DOIs	https://doi.org/10.3390/microorganisms8010121
State	Published - Jan 2020

Bibliographical note

Funding Information:
Supplementary Materials: Supplementary materials can be found at www.mdpi.com/xxx/s1. Author Contributions: Conceptualization, N.M.I., K.S., K.K., L.S. and V.C.; methodology, K.S., R.T., I.B. and J.J.L.M.; data curation, K.S., I.B., S.S., D.E., P.H., L.S. and V.C.; writing—original draft preparation, K.S., N.M.I., I.B., JC.Jo.Ln.cMep.,tRu.aTl.i,zLa.tSio. nan, Nd .VM.C.I..;,wKr.iSt.i,nKg—.Kr.,eLvi.eSw., aanndd Ved.Cit.i;nmg,eKth.So.d, oI.lBo.g, yR,.TK.,.SK.,. KR..,TP..,H I.B, L.,.aSn. adn Jd.MV..;Cd.;astua pceurrvaitsiioonn,, K.S., I.B., S.S., D.E., P.H., L.S., and V.C.; writing—original draft preparation, K.S., N.M.I., I.B., J.M., R.T., L.S., and V.C.; authors read and agreed to the published version of the manuscript. writing—review and editing, K.S., I.B., R.T., K.K., P.H., L.S., and V.C.; supervision, K.S., L.S., and V.C.; project Fadumndininisgt:raTthioisns, tKu.dSy., wK.aKs.s,uLp.Sp.o, artneddVby.Ct.h;eanMdinfuisntrdyinogf Eacdquuciastiitoionn, Y, Kou.Sth., Pan.Hd.,SapnodrtsVo.Cf t.he Czech Republic MSCA IF II project (CZ.02.2.69/0.0/0.0/18_070/0010493) and Czech Science foundation (GACˇ R)—Project No.19-17868Y). This research was also funded by Project “Campania Oncoterapie” No. B61G18000470007. Finally, the study was sMuSpCpoAr tIeFd IIb yprCorjeocsts-(BCoZr.d0e2r.2c.o69o/p0e.0ra/0ti.0o/n18C_z0e7c0h/–0B01a0v4a9r3ia)— anPdroCjezcetcNhoS.c4ie1n. ce foundation (GAČR)—Project No.19-17868Y). This research was also funded by Project “Campania Oncoterapie” No. B61G18000470007. Finally, the Acknowledgments: N.M.I., K.S. and K.K. would like to thank the management of VIT University for providing thestudyfacilitieswas suppto carryortedoutby Crosthis sstu-Bodyrder. cooperation Czech–Bavaria—Project No. 41.

Funding Information:
This study was supported by the Ministry of Education, Youth and Sports of the Czech Republic MSCA IF II project (CZ.02.2.69/0.0/0.0/18_070/0010493) and Czech Science foundation (GAČR)—Project No.19-17868Y). This research was also funded by Project “Campania Oncoterapie” No. B61G18000470007. Finally, the study was supported by Cross-Border cooperation Czech–Bavaria—Project No. 41.

Publisher Copyright:
© 2020 by the authors. Licensee MDPI, Basel, Switzerland.

Keywords

Actinobacteria
Biosynthetic gene clusters (BGCs)
Cyclic dipeptides (2,5-diketopiperazines, DKPs)
Global natural product social networking (GNPS)
LC-HRMS
Natural product
Quorum sensing inhibition (QSI)

ASJC Scopus subject areas

Microbiology
Microbiology (medical)
Virology

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10.3390/microorganisms8010121

Cite this

Ishaque, N. M., Burgsdorf, I., Malit, J. J. L., Saha, S., Teta, R., Ewe, D., Kannabiran, K., Hrouzek, P., Steindler, L., Costantino, V., & Saurav, K. (2020). Isolation, genomic and metabolomic characterization of Streptomyces tendae VITAKN with quorum sensing inhibitory activity from Southern India. Microorganisms, 8(1), [121]. https://doi.org/10.3390/microorganisms8010121

@article{a26f73599b20471a8793a61fae95b093,

title = "Isolation, genomic and metabolomic characterization of Streptomyces tendae VITAKN with quorum sensing inhibitory activity from Southern India",

abstract = "Streptomyces are among the most promising genera in terms of production ability to biosynthesize a variety of bioactive secondary metabolites with pharmaceutical interest. Coinciding with the increase in genomic sequencing of these bacteria, mining of their genomes for biosynthetic gene clusters (BGCs) has become a routine component of natural product discovery. Herein, we describe the isolation and characterization of a Streptomyces tendae VITAKN with quorum sensing inhibitory (QSI) activity that was isolated from southern coastal part of India. The nearly complete genome consists of 8,621,231bp with a GC content of 72.2%. Sequence similarity networks of the BGCs detected from this strain against the Minimum Information about a Biosynthetic Gene Cluster (MIBiG) database and 3365 BGCs predicted by antiSMASH analysis of publicly available complete Streptomyces genomes were generated through the BiG-SCAPE-CORASON platform to evaluate its biosynthetic novelty. Crude extract analysis using high-performance liquid chromatography connected to high resolution tandem mass spectrometry (HPLC-HRMS/MS) and dereplication through the Global Natural Product Social Molecular Networking (GNPS) online workflow resulted in the identification of cyclic dipeptides (2, 5-diketopiperazines, DKPs) in the extract, which are known to possess QSI activity. Our results highlight the potential of genome mining coupled with LC-HRMS/MS and in silico tools (GNPS) as a valid approach for the discovery of novel QSI lead compounds. This study also provides the biosynthetic diversity of BGCs and an assessment of the predicted chemical space yet to be discovered.",

keywords = "Actinobacteria, Biosynthetic gene clusters (BGCs), Cyclic dipeptides (2,5-diketopiperazines, DKPs), Global natural product social networking (GNPS), LC-HRMS, Natural product, Quorum sensing inhibition (QSI)",

author = "Ishaque, {Nabila Mohammed} and Ilia Burgsdorf and Malit, {Jessie James Limlingan} and Subhasish Saha and Roberta Teta and Daniela Ewe and Krishnan Kannabiran and Pavel Hrouzek and Laura Steindler and Valeria Costantino and Kumar Saurav",

note = "Funding Information: Supplementary Materials: Supplementary materials can be found at www.mdpi.com/xxx/s1. Author Contributions: Conceptualization, N.M.I., K.S., K.K., L.S. and V.C.; methodology, K.S., R.T., I.B. and J.J.L.M.; data curation, K.S., I.B., S.S., D.E., P.H., L.S. and V.C.; writing—original draft preparation, K.S., N.M.I., I.B., JC.Jo.Ln.cMep.,tRu.aTl.i,zLa.tSio. nan, Nd .VM.C.I..;,wKr.iSt.i,nKg—.Kr.,eLvi.eSw., aanndd Ved.Cit.i;nmg,eKth.So.d, oI.lBo.g, yR,.TK.,.SK.,. KR..,TP..,H I.B, L.,.aSn. adn Jd.MV..;Cd.;astua pceurrvaitsiioonn,, K.S., I.B., S.S., D.E., P.H., L.S., and V.C.; writing—original draft preparation, K.S., N.M.I., I.B., J.M., R.T., L.S., and V.C.; authors read and agreed to the published version of the manuscript. writing—review and editing, K.S., I.B., R.T., K.K., P.H., L.S., and V.C.; supervision, K.S., L.S., and V.C.; project Fadumndininisgt:raTthioisns, tKu.dSy., wK.aKs.s,uLp.Sp.o, artneddVby.Ct.h;eanMdinfuisntrdyinogf Eacdquuciastiitoionn, Y, Kou.Sth., Pan.Hd.,SapnodrtsVo.Cf t.he Czech Republic MSCA IF II project (CZ.02.2.69/0.0/0.0/18_070/0010493) and Czech Science foundation (GACˇ R)—Project No.19-17868Y). This research was also funded by Project “Campania Oncoterapie” No. B61G18000470007. Finally, the study was sMuSpCpoAr tIeFd IIb yprCorjeocsts-(BCoZr.d0e2r.2c.o69o/p0e.0ra/0ti.0o/n18C_z0e7c0h/–0B01a0v4a9r3ia)— anPdroCjezcetcNhoS.c4ie1n. ce foundation (GA{\v C}R)—Project No.19-17868Y). This research was also funded by Project “Campania Oncoterapie” No. B61G18000470007. Finally, the Acknowledgments: N.M.I., K.S. and K.K. would like to thank the management of VIT University for providing thestudyfacilitieswas suppto carryortedoutby Crosthis sstu-Bodyrder. cooperation Czech–Bavaria—Project No. 41. Funding Information: This study was supported by the Ministry of Education, Youth and Sports of the Czech Republic MSCA IF II project (CZ.02.2.69/0.0/0.0/18_070/0010493) and Czech Science foundation (GA{\v C}R)—Project No.19-17868Y). This research was also funded by Project “Campania Oncoterapie” No. B61G18000470007. Finally, the study was supported by Cross-Border cooperation Czech–Bavaria—Project No. 41. Publisher Copyright: {\textcopyright} 2020 by the authors. Licensee MDPI, Basel, Switzerland.",

year = "2020",

month = jan,

doi = "10.3390/microorganisms8010121",

language = "English",

volume = "8",

journal = "Microorganisms",

issn = "2076-2607",

publisher = "MDPI AG",

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TY - JOUR

T1 - Isolation, genomic and metabolomic characterization of Streptomyces tendae VITAKN with quorum sensing inhibitory activity from Southern India

AU - Ishaque, Nabila Mohammed

AU - Burgsdorf, Ilia

AU - Malit, Jessie James Limlingan

AU - Saha, Subhasish

AU - Teta, Roberta

AU - Ewe, Daniela

AU - Kannabiran, Krishnan

AU - Hrouzek, Pavel

AU - Steindler, Laura

AU - Costantino, Valeria

AU - Saurav, Kumar

N1 - Funding Information: Supplementary Materials: Supplementary materials can be found at www.mdpi.com/xxx/s1. Author Contributions: Conceptualization, N.M.I., K.S., K.K., L.S. and V.C.; methodology, K.S., R.T., I.B. and J.J.L.M.; data curation, K.S., I.B., S.S., D.E., P.H., L.S. and V.C.; writing—original draft preparation, K.S., N.M.I., I.B., JC.Jo.Ln.cMep.,tRu.aTl.i,zLa.tSio. nan, Nd .VM.C.I..;,wKr.iSt.i,nKg—.Kr.,eLvi.eSw., aanndd Ved.Cit.i;nmg,eKth.So.d, oI.lBo.g, yR,.TK.,.SK.,. KR..,TP..,H I.B, L.,.aSn. adn Jd.MV..;Cd.;astua pceurrvaitsiioonn,, K.S., I.B., S.S., D.E., P.H., L.S., and V.C.; writing—original draft preparation, K.S., N.M.I., I.B., J.M., R.T., L.S., and V.C.; authors read and agreed to the published version of the manuscript. writing—review and editing, K.S., I.B., R.T., K.K., P.H., L.S., and V.C.; supervision, K.S., L.S., and V.C.; project Fadumndininisgt:raTthioisns, tKu.dSy., wK.aKs.s,uLp.Sp.o, artneddVby.Ct.h;eanMdinfuisntrdyinogf Eacdquuciastiitoionn, Y, Kou.Sth., Pan.Hd.,SapnodrtsVo.Cf t.he Czech Republic MSCA IF II project (CZ.02.2.69/0.0/0.0/18_070/0010493) and Czech Science foundation (GACˇ R)—Project No.19-17868Y). This research was also funded by Project “Campania Oncoterapie” No. B61G18000470007. Finally, the study was sMuSpCpoAr tIeFd IIb yprCorjeocsts-(BCoZr.d0e2r.2c.o69o/p0e.0ra/0ti.0o/n18C_z0e7c0h/–0B01a0v4a9r3ia)— anPdroCjezcetcNhoS.c4ie1n. ce foundation (GAČR)—Project No.19-17868Y). This research was also funded by Project “Campania Oncoterapie” No. B61G18000470007. Finally, the Acknowledgments: N.M.I., K.S. and K.K. would like to thank the management of VIT University for providing thestudyfacilitieswas suppto carryortedoutby Crosthis sstu-Bodyrder. cooperation Czech–Bavaria—Project No. 41. Funding Information: This study was supported by the Ministry of Education, Youth and Sports of the Czech Republic MSCA IF II project (CZ.02.2.69/0.0/0.0/18_070/0010493) and Czech Science foundation (GAČR)—Project No.19-17868Y). This research was also funded by Project “Campania Oncoterapie” No. B61G18000470007. Finally, the study was supported by Cross-Border cooperation Czech–Bavaria—Project No. 41. Publisher Copyright: © 2020 by the authors. Licensee MDPI, Basel, Switzerland.

PY - 2020/1

Y1 - 2020/1

N2 - Streptomyces are among the most promising genera in terms of production ability to biosynthesize a variety of bioactive secondary metabolites with pharmaceutical interest. Coinciding with the increase in genomic sequencing of these bacteria, mining of their genomes for biosynthetic gene clusters (BGCs) has become a routine component of natural product discovery. Herein, we describe the isolation and characterization of a Streptomyces tendae VITAKN with quorum sensing inhibitory (QSI) activity that was isolated from southern coastal part of India. The nearly complete genome consists of 8,621,231bp with a GC content of 72.2%. Sequence similarity networks of the BGCs detected from this strain against the Minimum Information about a Biosynthetic Gene Cluster (MIBiG) database and 3365 BGCs predicted by antiSMASH analysis of publicly available complete Streptomyces genomes were generated through the BiG-SCAPE-CORASON platform to evaluate its biosynthetic novelty. Crude extract analysis using high-performance liquid chromatography connected to high resolution tandem mass spectrometry (HPLC-HRMS/MS) and dereplication through the Global Natural Product Social Molecular Networking (GNPS) online workflow resulted in the identification of cyclic dipeptides (2, 5-diketopiperazines, DKPs) in the extract, which are known to possess QSI activity. Our results highlight the potential of genome mining coupled with LC-HRMS/MS and in silico tools (GNPS) as a valid approach for the discovery of novel QSI lead compounds. This study also provides the biosynthetic diversity of BGCs and an assessment of the predicted chemical space yet to be discovered.

AB - Streptomyces are among the most promising genera in terms of production ability to biosynthesize a variety of bioactive secondary metabolites with pharmaceutical interest. Coinciding with the increase in genomic sequencing of these bacteria, mining of their genomes for biosynthetic gene clusters (BGCs) has become a routine component of natural product discovery. Herein, we describe the isolation and characterization of a Streptomyces tendae VITAKN with quorum sensing inhibitory (QSI) activity that was isolated from southern coastal part of India. The nearly complete genome consists of 8,621,231bp with a GC content of 72.2%. Sequence similarity networks of the BGCs detected from this strain against the Minimum Information about a Biosynthetic Gene Cluster (MIBiG) database and 3365 BGCs predicted by antiSMASH analysis of publicly available complete Streptomyces genomes were generated through the BiG-SCAPE-CORASON platform to evaluate its biosynthetic novelty. Crude extract analysis using high-performance liquid chromatography connected to high resolution tandem mass spectrometry (HPLC-HRMS/MS) and dereplication through the Global Natural Product Social Molecular Networking (GNPS) online workflow resulted in the identification of cyclic dipeptides (2, 5-diketopiperazines, DKPs) in the extract, which are known to possess QSI activity. Our results highlight the potential of genome mining coupled with LC-HRMS/MS and in silico tools (GNPS) as a valid approach for the discovery of novel QSI lead compounds. This study also provides the biosynthetic diversity of BGCs and an assessment of the predicted chemical space yet to be discovered.

KW - Actinobacteria

KW - Biosynthetic gene clusters (BGCs)

KW - Cyclic dipeptides (2,5-diketopiperazines, DKPs)

KW - Global natural product social networking (GNPS)

KW - LC-HRMS

KW - Natural product

KW - Quorum sensing inhibition (QSI)

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U2 - 10.3390/microorganisms8010121

DO - 10.3390/microorganisms8010121

M3 - Article

AN - SCOPUS:85079034551

VL - 8

JO - Microorganisms

JF - Microorganisms

SN - 2076-2607

IS - 1

M1 - 121

ER -

Isolation, genomic and metabolomic characterization of Streptomyces tendae VITAKN with quorum sensing inhibitory activity from Southern India

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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