Adaptive Evolution of <named-content content-type="genus-species">Geobacter sulfurreducens</named-content> in Coculture with <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>

ABSTRACT Interactions between microorganisms in mixed communities are highly complex, being either syntrophic, neutral, predatory, or competitive. Evolutionary changes can occur in the interaction dynamics between community members as they adapt to coexistence. Here, we report that the syntrophic in...

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Autores principales:	Lucie Semenec, Ismael A. Vergara, Andrew E. Laloo, Steve Petrovski, Philip L. Bond, Ashley E. Franks
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	competition evolution mutualism syntrophs Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/7a0da95d51e1468abba2dc85de305774
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spelling	oai:doaj.org-article:7a0da95d51e1468abba2dc85de3057742021-11-15T15:57:02ZAdaptive Evolution of <named-content content-type="genus-species">Geobacter sulfurreducens</named-content> in Coculture with <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>10.1128/mBio.02875-192150-7511https://doaj.org/article/7a0da95d51e1468abba2dc85de3057742020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02875-19https://doaj.org/toc/2150-7511ABSTRACT Interactions between microorganisms in mixed communities are highly complex, being either syntrophic, neutral, predatory, or competitive. Evolutionary changes can occur in the interaction dynamics between community members as they adapt to coexistence. Here, we report that the syntrophic interaction between Geobacter sulfurreducens and Pseudomonas aeruginosa coculture change in their dynamics over evolutionary time. Specifically, Geobacter sp. dominance increases with adaptation within the cocultures, as determined through quantitative PCR and fluorescence in situ hybridization. This suggests a transition from syntrophy to competition and demonstrates the rapid adaptive capacity of Geobacter spp. to dominate in cocultures with P. aeruginosa. Early in coculture establishment, two single-nucleotide variants in the G. sulfurreducens fabI and tetR genes emerged that were strongly selected for throughout coculture evolution with P. aeruginosa phenazine wild-type and phenazine-deficient mutants. Sequential window acquisition of all theoretical spectra-mass spectrometry (SWATH-MS) proteomics revealed that the tetR variant cooccurred with the upregulation of an adenylate cyclase transporter, CyaE, and a resistance-nodulation-division (RND) efflux pump notably known for antibiotic efflux. To determine whether antibiotic production was driving the increased expression of the multidrug efflux pump, we tested Pseudomonas-derived phenazine-1-carboxylic acid (PHZ-1-CA) for its potential to inhibit Geobacter growth and drive selection of the tetR and fabI genetic variants. Despite its inhibitory properties, PHZ-1-CA did not drive variant selection, indicating that other antibiotics may drive overexpression of the efflux pump and CyaE or that a novel role exists for these proteins in the context of this interaction. IMPORTANCE Geobacter and Pseudomonas spp. cohabit many of the same environments, where Geobacter spp. often dominate. Both bacteria are capable of extracellular electron transfer (EET) and play important roles in biogeochemical cycling. Although they recently in 2017 were demonstrated to undergo direct interspecies electron transfer (DIET) with one another, the genetic evolution of this syntrophic interaction has not been examined. Here, we use whole-genome sequencing of the cocultures before and after adaptive evolution to determine whether genetic selection is occurring. We also probe their interaction on a temporal level and determine whether their interaction dynamics change over the course of adaptive evolution. This study brings to light the multifaceted nature of interactions between just two microorganisms within a controlled environment and will aid in improving metabolic models of microbial communities comprising these two bacteria.Lucie SemenecIsmael A. VergaraAndrew E. LalooSteve PetrovskiPhilip L. BondAshley E. FranksAmerican Society for MicrobiologyarticlecompetitionevolutionmutualismsyntrophsMicrobiologyQR1-502ENmBio, Vol 11, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	competition evolution mutualism syntrophs Microbiology QR1-502
spellingShingle	competition evolution mutualism syntrophs Microbiology QR1-502 Lucie Semenec Ismael A. Vergara Andrew E. Laloo Steve Petrovski Philip L. Bond Ashley E. Franks Adaptive Evolution of <named-content content-type="genus-species">Geobacter sulfurreducens</named-content> in Coculture with <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
description	ABSTRACT Interactions between microorganisms in mixed communities are highly complex, being either syntrophic, neutral, predatory, or competitive. Evolutionary changes can occur in the interaction dynamics between community members as they adapt to coexistence. Here, we report that the syntrophic interaction between Geobacter sulfurreducens and Pseudomonas aeruginosa coculture change in their dynamics over evolutionary time. Specifically, Geobacter sp. dominance increases with adaptation within the cocultures, as determined through quantitative PCR and fluorescence in situ hybridization. This suggests a transition from syntrophy to competition and demonstrates the rapid adaptive capacity of Geobacter spp. to dominate in cocultures with P. aeruginosa. Early in coculture establishment, two single-nucleotide variants in the G. sulfurreducens fabI and tetR genes emerged that were strongly selected for throughout coculture evolution with P. aeruginosa phenazine wild-type and phenazine-deficient mutants. Sequential window acquisition of all theoretical spectra-mass spectrometry (SWATH-MS) proteomics revealed that the tetR variant cooccurred with the upregulation of an adenylate cyclase transporter, CyaE, and a resistance-nodulation-division (RND) efflux pump notably known for antibiotic efflux. To determine whether antibiotic production was driving the increased expression of the multidrug efflux pump, we tested Pseudomonas-derived phenazine-1-carboxylic acid (PHZ-1-CA) for its potential to inhibit Geobacter growth and drive selection of the tetR and fabI genetic variants. Despite its inhibitory properties, PHZ-1-CA did not drive variant selection, indicating that other antibiotics may drive overexpression of the efflux pump and CyaE or that a novel role exists for these proteins in the context of this interaction. IMPORTANCE Geobacter and Pseudomonas spp. cohabit many of the same environments, where Geobacter spp. often dominate. Both bacteria are capable of extracellular electron transfer (EET) and play important roles in biogeochemical cycling. Although they recently in 2017 were demonstrated to undergo direct interspecies electron transfer (DIET) with one another, the genetic evolution of this syntrophic interaction has not been examined. Here, we use whole-genome sequencing of the cocultures before and after adaptive evolution to determine whether genetic selection is occurring. We also probe their interaction on a temporal level and determine whether their interaction dynamics change over the course of adaptive evolution. This study brings to light the multifaceted nature of interactions between just two microorganisms within a controlled environment and will aid in improving metabolic models of microbial communities comprising these two bacteria.
format	article
author	Lucie Semenec Ismael A. Vergara Andrew E. Laloo Steve Petrovski Philip L. Bond Ashley E. Franks
author_facet	Lucie Semenec Ismael A. Vergara Andrew E. Laloo Steve Petrovski Philip L. Bond Ashley E. Franks
author_sort	Lucie Semenec
title	Adaptive Evolution of <named-content content-type="genus-species">Geobacter sulfurreducens</named-content> in Coculture with <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_short	Adaptive Evolution of <named-content content-type="genus-species">Geobacter sulfurreducens</named-content> in Coculture with <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_full	Adaptive Evolution of <named-content content-type="genus-species">Geobacter sulfurreducens</named-content> in Coculture with <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_fullStr	Adaptive Evolution of <named-content content-type="genus-species">Geobacter sulfurreducens</named-content> in Coculture with <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_full_unstemmed	Adaptive Evolution of <named-content content-type="genus-species">Geobacter sulfurreducens</named-content> in Coculture with <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_sort	adaptive evolution of <named-content content-type="genus-species">geobacter sulfurreducens</named-content> in coculture with <named-content content-type="genus-species">pseudomonas aeruginosa</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/7a0da95d51e1468abba2dc85de305774
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Adaptive Evolution of <named-content content-type="genus-species">Geobacter sulfurreducens</named-content> in Coculture with <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>

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