Identification of quorum sensing activators and inhibitors in the marine sponge sarcotragus spinosulus

Kumar Saurav, Nicola Borbone, Ilia Burgsdorf, Roberta Teta, Alessia Caso, Rinat Bar-Shalom, Germana Esposito, Maya Britstein, Laura Steindler, Valeria Costantino

Research output: Contribution to journalArticlepeer-review

Abstract

Marine sponges, a well-documented prolific source of natural products, harbor highly diverse microbial communities. Their extracts were previously shown to contain quorum sensing (QS) signal molecules of the N-acyl homoserine lactone (AHL) type, known to orchestrate bacterial gene regulation. Some bacteria and eukaryotic organisms are known to produce molecules that can interfere with QS signaling, thus affecting microbial genetic regulation and function. In the present study, we established the production of both QS signal molecules as well as QS inhibitory (QSI) molecules in the sponge species Sarcotragus spinosulus. A total of eighteen saturated acyl chain AHLs were identified along with six unsaturated acyl chain AHLs. Bioassay-guided purification led to the isolation of two brominated metabolites with QSI activity. The structures of these compounds were elucidated by comparative spectral analysis of 1HNMR and HR-MS data and were identified as 3-bromo-4-methoxyphenethylamine (1) and 5,6-dibromo-N,N-dimethyltryptamine (2). The QSI activity of compounds 1 and 2 was evaluated using reporter gene assays for long- and short-chain AHL signals (Escherichia coli pSB1075 and E. coli pSB401, respectively). QSI activity was further confirmed by measuring dose-dependent inhibition of proteolytic activity and pyocyanin production in Pseudomonas aeruginosa PAO1. The obtained results show the coexistence of QS and QSI in S. spinosulus, a complex signal network that may mediate the orchestrated function of the microbiome within the sponge holobiont.

Original languageEnglish
Article number18020127
JournalMarine Drugs
Volume18
Issue number2
DOIs
StatePublished - 2020

Bibliographical note

Funding Information:
This study was supported by the Israel Science Foundation [grant no. 1243/16] titled “Identification of molecular mechanisms underlying sponge-microbiome symbiosis” and the “Programma Sostegno Territorialeal leattività di ricerca (STAR)”, Università degli Studi di Napoli Federico II (UNINA) Project entitled 'SeaLeads'. K.S. had a post-doctoral fellowship from the Israeli Council for Higher Education (VATAT) and the University of Haifa. K.S. post-doctoral fellowship was also supported by the Università degli Studi di Napoli Federico II, bilateral agreement Haifa-Naples 2015-2018. This research was also funded by Regione Campania, PO FESR 2014-2020, O.S. 1.2, Project “Campania Oncoterapie” No. B61G18000470007. We would like to thank Markus Haber and the Staff at the Morris Khan Marine Research Station for support with the diving activities during this study. Sponge samples were collected in compliance with permits 2012/38390 and 2013/38920 from the Israel Nature and National Parks Protection Authority.

Funding Information:
Funding: This study was supported by the Israel Science Foundation [grant no. 1243/16] titled “Identification of molecular mechanisms underlying sponge-microbiome symbiosis” and the “Programma Sostegno Territorialeal leattività di ricerca (STAR)”, Università degli Studi di Napoli Federico II (UNINA) Project entitled ‘SeaLeads’. K.S. had a post-doctoral fellowship from the Israeli Council for Higher Education (VATAT) and the University of Haifa. K.S. post-doctoral fellowship was also supported by the Università degli Studi di Napoli Federico II, bilateral agreement Haifa-Naples 2015-2018. This research was also funded by Regione Campania, PO FESR 2014-2020, O.S. 1.2, Project “Campania Oncoterapie” No. B61G18000470007.

Publisher Copyright:
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).

Keywords

  • 3-bromo-4-methoxyphenethylamine
  • 5
  • 6-dibromo-N
  • N-acyl homoserine lactone
  • N-dimethyltryptamine
  • Quorum sensing
  • Quorum sensing inhibition
  • Sarcotragus spinosulus
  • Sponge

ASJC Scopus subject areas

  • Drug Discovery

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