The Quorum Sensing Auto-Inducer 2 (AI-2) Stimulates Nitrogen Fixation and Favors Ethanol Production over Biomass Accumulation in <i>Zymomonas mobilis</i>

Autoinducer 2 (or AI-2) is one of the molecules used by bacteria to trigger the Quorum Sensing (QS) response, which activates expression of genes involved in a series of alternative mechanisms, when cells reach high population densities (including bioluminescence, motility, biofilm formation, stress...

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Main Authors: Valquíria Campos Alencar, Juliana de Fátima dos Santos Silva, Renata Ozelami Vilas Boas, Vinícius Manganaro Farnézio, Yara N. L. F. de Maria, David Aciole Barbosa, Alex Tramontin Almeida, Emanuel Maltempi de Souza, Marcelo Müller-Santos, Daniela L. Jabes, Fabiano B. Menegidio, Regina Costa de Oliveira, Tiago Rodrigues, Ivarne Luis dos Santos Tersariol, Adrian R. Walmsley, Luiz R. Nunes
Format: Article
Language:English
Published: MDPI AG 2021-05-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/22/11/5628
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language English
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author Valquíria Campos Alencar
Juliana de Fátima dos Santos Silva
Renata Ozelami Vilas Boas
Vinícius Manganaro Farnézio
Yara N. L. F. de Maria
David Aciole Barbosa
Alex Tramontin Almeida
Emanuel Maltempi de Souza
Marcelo Müller-Santos
Daniela L. Jabes
Fabiano B. Menegidio
Regina Costa de Oliveira
Tiago Rodrigues
Ivarne Luis dos Santos Tersariol
Adrian R. Walmsley
Luiz R. Nunes
spellingShingle Valquíria Campos Alencar
Juliana de Fátima dos Santos Silva
Renata Ozelami Vilas Boas
Vinícius Manganaro Farnézio
Yara N. L. F. de Maria
David Aciole Barbosa
Alex Tramontin Almeida
Emanuel Maltempi de Souza
Marcelo Müller-Santos
Daniela L. Jabes
Fabiano B. Menegidio
Regina Costa de Oliveira
Tiago Rodrigues
Ivarne Luis dos Santos Tersariol
Adrian R. Walmsley
Luiz R. Nunes
The Quorum Sensing Auto-Inducer 2 (AI-2) Stimulates Nitrogen Fixation and Favors Ethanol Production over Biomass Accumulation in <i>Zymomonas mobilis</i>
International Journal of Molecular Sciences
<i>Zymomonas mobilis</i>
quorum sensing
AI-2
N<sub>2</sub> fixation
ethanol production
transcriptome
author_facet Valquíria Campos Alencar
Juliana de Fátima dos Santos Silva
Renata Ozelami Vilas Boas
Vinícius Manganaro Farnézio
Yara N. L. F. de Maria
David Aciole Barbosa
Alex Tramontin Almeida
Emanuel Maltempi de Souza
Marcelo Müller-Santos
Daniela L. Jabes
Fabiano B. Menegidio
Regina Costa de Oliveira
Tiago Rodrigues
Ivarne Luis dos Santos Tersariol
Adrian R. Walmsley
Luiz R. Nunes
author_sort Valquíria Campos Alencar
title The Quorum Sensing Auto-Inducer 2 (AI-2) Stimulates Nitrogen Fixation and Favors Ethanol Production over Biomass Accumulation in <i>Zymomonas mobilis</i>
title_short The Quorum Sensing Auto-Inducer 2 (AI-2) Stimulates Nitrogen Fixation and Favors Ethanol Production over Biomass Accumulation in <i>Zymomonas mobilis</i>
title_full The Quorum Sensing Auto-Inducer 2 (AI-2) Stimulates Nitrogen Fixation and Favors Ethanol Production over Biomass Accumulation in <i>Zymomonas mobilis</i>
title_fullStr The Quorum Sensing Auto-Inducer 2 (AI-2) Stimulates Nitrogen Fixation and Favors Ethanol Production over Biomass Accumulation in <i>Zymomonas mobilis</i>
title_full_unstemmed The Quorum Sensing Auto-Inducer 2 (AI-2) Stimulates Nitrogen Fixation and Favors Ethanol Production over Biomass Accumulation in <i>Zymomonas mobilis</i>
title_sort quorum sensing auto-inducer 2 (ai-2) stimulates nitrogen fixation and favors ethanol production over biomass accumulation in <i>zymomonas mobilis</i>
publisher MDPI AG
series International Journal of Molecular Sciences
issn 1661-6596
1422-0067
publishDate 2021-05-01
description Autoinducer 2 (or AI-2) is one of the molecules used by bacteria to trigger the Quorum Sensing (QS) response, which activates expression of genes involved in a series of alternative mechanisms, when cells reach high population densities (including bioluminescence, motility, biofilm formation, stress resistance, and production of public goods, or pathogenicity factors, among others). Contrary to most autoinducers, AI-2 can induce QS responses in both Gram-negative and Gram-positive bacteria, and has been suggested to constitute a trans-specific system of bacterial communication, capable of affecting even bacteria that cannot produce this autoinducer. In this work, we demonstrate that the ethanologenic Gram-negative bacterium <i>Zymomonas mobilis</i> (a non-AI-2 producer) responds to exogenous AI-2 by modulating expression of genes involved in mechanisms typically associated with QS in other bacteria, such as motility, DNA repair, and nitrogen fixation. Interestingly, the metabolism of AI-2-induced <i>Z. mobilis</i> cells seems to favor ethanol production over biomass accumulation, probably as an adaptation to the high-energy demand of N<sub>2</sub> fixation. This opens the possibility of employing AI-2 during the industrial production of second-generation ethanol, as a way to boost N<sub>2</sub> fixation by these bacteria, which could reduce costs associated with the use of nitrogen-based fertilizers, without compromising ethanol production in industrial plants.
topic <i>Zymomonas mobilis</i>
quorum sensing
AI-2
N<sub>2</sub> fixation
ethanol production
transcriptome
url https://www.mdpi.com/1422-0067/22/11/5628
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spelling doaj-2e6a2261cce2496483a40217f3a698cf2021-06-01T01:07:36ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-05-01225628562810.3390/ijms22115628The Quorum Sensing Auto-Inducer 2 (AI-2) Stimulates Nitrogen Fixation and Favors Ethanol Production over Biomass Accumulation in <i>Zymomonas mobilis</i>Valquíria Campos Alencar0Juliana de Fátima dos Santos Silva1Renata Ozelami Vilas Boas2Vinícius Manganaro Farnézio3Yara N. L. F. de Maria4David Aciole Barbosa5Alex Tramontin Almeida6Emanuel Maltempi de Souza7Marcelo Müller-Santos8Daniela L. Jabes9Fabiano B. Menegidio10Regina Costa de Oliveira11Tiago Rodrigues12Ivarne Luis dos Santos Tersariol13Adrian R. Walmsley14Luiz R. Nunes15Centro de Ciências Naturais e Humanas, Universidade Federal do ABC (UFABC), Alameda da Universidade, s/n, São Bernardo do Campo 09606-045, SP, BrazilCentro de Ciências Naturais e Humanas, Universidade Federal do ABC (UFABC), Alameda da Universidade, s/n, São Bernardo do Campo 09606-045, SP, BrazilNúcleo Integrado de Biotecnologia, Universidade de Mogi das Cruzes (UMC), Av. Dr. Cândido Xavier de Almeida Souza, 200, Mogi das Cruzes 08780-911, SP, BrazilCentro de Ciências Naturais e Humanas, Universidade Federal do ABC (UFABC), Alameda da Universidade, s/n, São Bernardo do Campo 09606-045, SP, BrazilNúcleo Integrado de Biotecnologia, Universidade de Mogi das Cruzes (UMC), Av. Dr. Cândido Xavier de Almeida Souza, 200, Mogi das Cruzes 08780-911, SP, BrazilNúcleo Integrado de Biotecnologia, Universidade de Mogi das Cruzes (UMC), Av. Dr. Cândido Xavier de Almeida Souza, 200, Mogi das Cruzes 08780-911, SP, BrazilSetor de Ciências Biológicas-Departamento de Bioquímica e Biologia Molecular, Universidade Federal do Paraná (UFPR), Rua Cel. Francisco H. dos Santos, 100, Curitiba 81531-980, PR, BrazilSetor de Ciências Biológicas-Departamento de Bioquímica e Biologia Molecular, Universidade Federal do Paraná (UFPR), Rua Cel. Francisco H. dos Santos, 100, Curitiba 81531-980, PR, BrazilSetor de Ciências Biológicas-Departamento de Bioquímica e Biologia Molecular, Universidade Federal do Paraná (UFPR), Rua Cel. Francisco H. dos Santos, 100, Curitiba 81531-980, PR, BrazilNúcleo Integrado de Biotecnologia, Universidade de Mogi das Cruzes (UMC), Av. Dr. Cândido Xavier de Almeida Souza, 200, Mogi das Cruzes 08780-911, SP, BrazilNúcleo Integrado de Biotecnologia, Universidade de Mogi das Cruzes (UMC), Av. Dr. Cândido Xavier de Almeida Souza, 200, Mogi das Cruzes 08780-911, SP, BrazilNúcleo Integrado de Biotecnologia, Universidade de Mogi das Cruzes (UMC), Av. Dr. Cândido Xavier de Almeida Souza, 200, Mogi das Cruzes 08780-911, SP, BrazilCentro de Ciências Naturais e Humanas, Universidade Federal do ABC (UFABC), Alameda da Universidade, s/n, São Bernardo do Campo 09606-045, SP, BrazilDepartamento de Bioquímica, Universidade Federal de São Paulo (UNIFESP), Rua Três de Maio, 100, São Paulo 04044-020, SP, BrazilDepartment of Biosciences, Durham University, South Road, Durham DH1 3LE, UKCentro de Ciências Naturais e Humanas, Universidade Federal do ABC (UFABC), Alameda da Universidade, s/n, São Bernardo do Campo 09606-045, SP, BrazilAutoinducer 2 (or AI-2) is one of the molecules used by bacteria to trigger the Quorum Sensing (QS) response, which activates expression of genes involved in a series of alternative mechanisms, when cells reach high population densities (including bioluminescence, motility, biofilm formation, stress resistance, and production of public goods, or pathogenicity factors, among others). Contrary to most autoinducers, AI-2 can induce QS responses in both Gram-negative and Gram-positive bacteria, and has been suggested to constitute a trans-specific system of bacterial communication, capable of affecting even bacteria that cannot produce this autoinducer. In this work, we demonstrate that the ethanologenic Gram-negative bacterium <i>Zymomonas mobilis</i> (a non-AI-2 producer) responds to exogenous AI-2 by modulating expression of genes involved in mechanisms typically associated with QS in other bacteria, such as motility, DNA repair, and nitrogen fixation. Interestingly, the metabolism of AI-2-induced <i>Z. mobilis</i> cells seems to favor ethanol production over biomass accumulation, probably as an adaptation to the high-energy demand of N<sub>2</sub> fixation. This opens the possibility of employing AI-2 during the industrial production of second-generation ethanol, as a way to boost N<sub>2</sub> fixation by these bacteria, which could reduce costs associated with the use of nitrogen-based fertilizers, without compromising ethanol production in industrial plants.https://www.mdpi.com/1422-0067/22/11/5628<i>Zymomonas mobilis</i>quorum sensingAI-2N<sub>2</sub> fixationethanol productiontranscriptome