Proteomic Analysis of a Syntrophic Coculture of Syntrophobacter fumaroxidans MPOBT and Geobacter sulfurreducens PCAT

We established a syntrophic coculture of Syntrophobacter fumaroxidans MPOBT (SF) and Geobacter sulfurreducens PCAT (GS) growing on propionate and Fe(III). Neither of the bacteria was capable of growth on propionate and Fe(III) in pure culture. Propionate degradation by SF provides acetate, hydrogen,...

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Autores principales: Monir Mollaei, Maria Suarez-Diez, Vicente T. Sedano-Nunez, Sjef Boeren, Alfons J. M. Stams, Caroline M. Plugge
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Publicado: Frontiers Media S.A. 2021
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spelling oai:doaj.org-article:7e3f855e6fa94753918a97a03e84d9442021-12-01T18:11:33ZProteomic Analysis of a Syntrophic Coculture of Syntrophobacter fumaroxidans MPOBT and Geobacter sulfurreducens PCAT1664-302X10.3389/fmicb.2021.708911https://doaj.org/article/7e3f855e6fa94753918a97a03e84d9442021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fmicb.2021.708911/fullhttps://doaj.org/toc/1664-302XWe established a syntrophic coculture of Syntrophobacter fumaroxidans MPOBT (SF) and Geobacter sulfurreducens PCAT (GS) growing on propionate and Fe(III). Neither of the bacteria was capable of growth on propionate and Fe(III) in pure culture. Propionate degradation by SF provides acetate, hydrogen, and/or formate that can be used as electron donors by GS with Fe(III) citrate as electron acceptor. Proteomic analyses of the SF-GS coculture revealed propionate conversion via the methylmalonyl-CoA (MMC) pathway by SF. The possibility of interspecies electron transfer (IET) via direct (DIET) and/or hydrogen/formate transfer (HFIT) was investigated by comparing the differential abundance of associated proteins in SF-GS coculture against (i) SF coculture with Methanospirillum hungatei (SF-MH), which relies on HFIT, (ii) GS pure culture growing on acetate, formate, hydrogen as propionate products, and Fe(III). We noted some evidence for DIET in the SF-GS coculture, i.e., GS in the coculture showed significantly lower abundance of uptake hydrogenase (43-fold) and formate dehydrogenase (45-fold) and significantly higher abundance of proteins related to acetate metabolism (i.e., GltA; 62-fold) compared to GS pure culture. Moreover, SF in the SF-GS coculture showed significantly lower abundance of IET-related formate dehydrogenases, Fdh3 (51-fold) and Fdh5 (29-fold), and the rate of propionate conversion in SF-GS was 8-fold lower than in the SF-MH coculture. In contrast, compared to GS pure culture, we found lower abundance of pilus-associated cytochrome OmcS (2-fold) and piliA (5-fold) in the SF-GS coculture that is suggested to be necessary for DIET. Furthermore, neither visible aggregates formed in the SF-GS coculture, nor the pili-E of SF (suggested as e-pili) were detected. These findings suggest that the IET mechanism is complex in the SF-GS coculture and can be mediated by several mechanisms rather than one discrete pathway. Our study can be further useful in understanding syntrophic propionate degradation in bioelectrochemical and anaerobic digestion systems.Monir MollaeiMonir MollaeiMaria Suarez-DiezVicente T. Sedano-NunezSjef BoerenAlfons J. M. StamsAlfons J. M. StamsCaroline M. PluggeCaroline M. PluggeFrontiers Media S.A.articleSyntrophobacter fumaroxidansGeobacter sulfurreducenscocultureinterspecies electron transferpropionateproteomicsMicrobiologyQR1-502ENFrontiers in Microbiology, Vol 12 (2021)
institution DOAJ
collection DOAJ
language EN
topic Syntrophobacter fumaroxidans
Geobacter sulfurreducens
coculture
interspecies electron transfer
propionate
proteomics
Microbiology
QR1-502
spellingShingle Syntrophobacter fumaroxidans
Geobacter sulfurreducens
coculture
interspecies electron transfer
propionate
proteomics
Microbiology
QR1-502
Monir Mollaei
Monir Mollaei
Maria Suarez-Diez
Vicente T. Sedano-Nunez
Sjef Boeren
Alfons J. M. Stams
Alfons J. M. Stams
Caroline M. Plugge
Caroline M. Plugge
Proteomic Analysis of a Syntrophic Coculture of Syntrophobacter fumaroxidans MPOBT and Geobacter sulfurreducens PCAT
description We established a syntrophic coculture of Syntrophobacter fumaroxidans MPOBT (SF) and Geobacter sulfurreducens PCAT (GS) growing on propionate and Fe(III). Neither of the bacteria was capable of growth on propionate and Fe(III) in pure culture. Propionate degradation by SF provides acetate, hydrogen, and/or formate that can be used as electron donors by GS with Fe(III) citrate as electron acceptor. Proteomic analyses of the SF-GS coculture revealed propionate conversion via the methylmalonyl-CoA (MMC) pathway by SF. The possibility of interspecies electron transfer (IET) via direct (DIET) and/or hydrogen/formate transfer (HFIT) was investigated by comparing the differential abundance of associated proteins in SF-GS coculture against (i) SF coculture with Methanospirillum hungatei (SF-MH), which relies on HFIT, (ii) GS pure culture growing on acetate, formate, hydrogen as propionate products, and Fe(III). We noted some evidence for DIET in the SF-GS coculture, i.e., GS in the coculture showed significantly lower abundance of uptake hydrogenase (43-fold) and formate dehydrogenase (45-fold) and significantly higher abundance of proteins related to acetate metabolism (i.e., GltA; 62-fold) compared to GS pure culture. Moreover, SF in the SF-GS coculture showed significantly lower abundance of IET-related formate dehydrogenases, Fdh3 (51-fold) and Fdh5 (29-fold), and the rate of propionate conversion in SF-GS was 8-fold lower than in the SF-MH coculture. In contrast, compared to GS pure culture, we found lower abundance of pilus-associated cytochrome OmcS (2-fold) and piliA (5-fold) in the SF-GS coculture that is suggested to be necessary for DIET. Furthermore, neither visible aggregates formed in the SF-GS coculture, nor the pili-E of SF (suggested as e-pili) were detected. These findings suggest that the IET mechanism is complex in the SF-GS coculture and can be mediated by several mechanisms rather than one discrete pathway. Our study can be further useful in understanding syntrophic propionate degradation in bioelectrochemical and anaerobic digestion systems.
format article
author Monir Mollaei
Monir Mollaei
Maria Suarez-Diez
Vicente T. Sedano-Nunez
Sjef Boeren
Alfons J. M. Stams
Alfons J. M. Stams
Caroline M. Plugge
Caroline M. Plugge
author_facet Monir Mollaei
Monir Mollaei
Maria Suarez-Diez
Vicente T. Sedano-Nunez
Sjef Boeren
Alfons J. M. Stams
Alfons J. M. Stams
Caroline M. Plugge
Caroline M. Plugge
author_sort Monir Mollaei
title Proteomic Analysis of a Syntrophic Coculture of Syntrophobacter fumaroxidans MPOBT and Geobacter sulfurreducens PCAT
title_short Proteomic Analysis of a Syntrophic Coculture of Syntrophobacter fumaroxidans MPOBT and Geobacter sulfurreducens PCAT
title_full Proteomic Analysis of a Syntrophic Coculture of Syntrophobacter fumaroxidans MPOBT and Geobacter sulfurreducens PCAT
title_fullStr Proteomic Analysis of a Syntrophic Coculture of Syntrophobacter fumaroxidans MPOBT and Geobacter sulfurreducens PCAT
title_full_unstemmed Proteomic Analysis of a Syntrophic Coculture of Syntrophobacter fumaroxidans MPOBT and Geobacter sulfurreducens PCAT
title_sort proteomic analysis of a syntrophic coculture of syntrophobacter fumaroxidans mpobt and geobacter sulfurreducens pcat
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/7e3f855e6fa94753918a97a03e84d944
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