The Effect of Secondary Metabolites Produced by Serratia marcescens on Aedes aegypti and Its Microbiota

Serratia marcescens is a bacterial species widely found in the environment, which very efficiently colonizes mosquitoes. In this study, we isolated a red-pigmented S. marcescens strain from our mosquito colony (called S. marcescens VA). This red pigmentation is caused by the production of prodigiosi...

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Main Authors: Katy Heu, Ottavia Romoli, Johan Claes Schönbeck, Rachel Ajenoe, Yanouk Epelboin, Verena Kircher, Emeline Houël, Yannick Estevez, Mathilde Gendrin
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.645701/full
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author Katy Heu
Ottavia Romoli
Johan Claes Schönbeck
Rachel Ajenoe
Yanouk Epelboin
Verena Kircher
Emeline Houël
Yannick Estevez
Mathilde Gendrin
Mathilde Gendrin
author_facet Katy Heu
Ottavia Romoli
Johan Claes Schönbeck
Rachel Ajenoe
Yanouk Epelboin
Verena Kircher
Emeline Houël
Yannick Estevez
Mathilde Gendrin
Mathilde Gendrin
author_sort Katy Heu
collection DOAJ
description Serratia marcescens is a bacterial species widely found in the environment, which very efficiently colonizes mosquitoes. In this study, we isolated a red-pigmented S. marcescens strain from our mosquito colony (called S. marcescens VA). This red pigmentation is caused by the production of prodigiosin, a molecule with antibacterial properties. To investigate the role of prodigiosin on mosquito-S. marcescens interactions, we produced two white mutants of S. marcescens VA by random mutagenesis. Whole genome sequencing and chemical analyses suggest that one mutant has a nonsense mutation in the gene encoding prodigiosin synthase, while the other one is deficient in the production of several types of secondary metabolites including prodigiosin and serratamolide. We used our mutants to investigate how S. marcescens secondary metabolites affect the mosquito and its microbiota. Our in vitro tests indicated that S. marcescens VA inhibits the growth of several mosquito microbiota isolates using a combination of prodigiosin and other secondary metabolites, corroborating published data. This strain requires secondary metabolites other than prodigiosin for its proteolytic and hemolytic activities. In the mosquito, we observed that S. marcescens VA is highly virulent to larvae in a prodigiosin-dependent manner, while its virulence on adults is lower and largely depends on other metabolites.
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spelling doaj.art-0635f7752e954164946be4f7855fad772022-12-21T22:53:57ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-07-011210.3389/fmicb.2021.645701645701The Effect of Secondary Metabolites Produced by Serratia marcescens on Aedes aegypti and Its MicrobiotaKaty Heu0Ottavia Romoli1Johan Claes Schönbeck2Rachel Ajenoe3Yanouk Epelboin4Verena Kircher5Emeline Houël6Yannick Estevez7Mathilde Gendrin8Mathilde Gendrin9Microbiota of Insect Vectors Group, Institut Pasteur de la Guyane, Cayenne, FranceMicrobiota of Insect Vectors Group, Institut Pasteur de la Guyane, Cayenne, FranceMicrobiota of Insect Vectors Group, Institut Pasteur de la Guyane, Cayenne, FranceMicrobiota of Insect Vectors Group, Institut Pasteur de la Guyane, Cayenne, FranceMicrobiota of Insect Vectors Group, Institut Pasteur de la Guyane, Cayenne, FranceMicrobiota of Insect Vectors Group, Institut Pasteur de la Guyane, Cayenne, FranceCNRS, UMR EcoFoG, AgroParisTech, Cirad, INRAE, Université des Antilles, Université de Guyane, Cayenne, FranceCNRS, UMR EcoFoG, AgroParisTech, Cirad, INRAE, Université des Antilles, Université de Guyane, Cayenne, FranceMicrobiota of Insect Vectors Group, Institut Pasteur de la Guyane, Cayenne, FranceParasites and Insect Vectors Department, Institut Pasteur, Paris, FranceSerratia marcescens is a bacterial species widely found in the environment, which very efficiently colonizes mosquitoes. In this study, we isolated a red-pigmented S. marcescens strain from our mosquito colony (called S. marcescens VA). This red pigmentation is caused by the production of prodigiosin, a molecule with antibacterial properties. To investigate the role of prodigiosin on mosquito-S. marcescens interactions, we produced two white mutants of S. marcescens VA by random mutagenesis. Whole genome sequencing and chemical analyses suggest that one mutant has a nonsense mutation in the gene encoding prodigiosin synthase, while the other one is deficient in the production of several types of secondary metabolites including prodigiosin and serratamolide. We used our mutants to investigate how S. marcescens secondary metabolites affect the mosquito and its microbiota. Our in vitro tests indicated that S. marcescens VA inhibits the growth of several mosquito microbiota isolates using a combination of prodigiosin and other secondary metabolites, corroborating published data. This strain requires secondary metabolites other than prodigiosin for its proteolytic and hemolytic activities. In the mosquito, we observed that S. marcescens VA is highly virulent to larvae in a prodigiosin-dependent manner, while its virulence on adults is lower and largely depends on other metabolites.https://www.frontiersin.org/articles/10.3389/fmicb.2021.645701/fullSerratiaAedes aegyptisecondary metaboliteprodigiosinmicrobiotaserratamolide
spellingShingle Katy Heu
Ottavia Romoli
Johan Claes Schönbeck
Rachel Ajenoe
Yanouk Epelboin
Verena Kircher
Emeline Houël
Yannick Estevez
Mathilde Gendrin
Mathilde Gendrin
The Effect of Secondary Metabolites Produced by Serratia marcescens on Aedes aegypti and Its Microbiota
Frontiers in Microbiology
Serratia
Aedes aegypti
secondary metabolite
prodigiosin
microbiota
serratamolide
title The Effect of Secondary Metabolites Produced by Serratia marcescens on Aedes aegypti and Its Microbiota
title_full The Effect of Secondary Metabolites Produced by Serratia marcescens on Aedes aegypti and Its Microbiota
title_fullStr The Effect of Secondary Metabolites Produced by Serratia marcescens on Aedes aegypti and Its Microbiota
title_full_unstemmed The Effect of Secondary Metabolites Produced by Serratia marcescens on Aedes aegypti and Its Microbiota
title_short The Effect of Secondary Metabolites Produced by Serratia marcescens on Aedes aegypti and Its Microbiota
title_sort effect of secondary metabolites produced by serratia marcescens on aedes aegypti and its microbiota
topic Serratia
Aedes aegypti
secondary metabolite
prodigiosin
microbiota
serratamolide
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.645701/full
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