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

Monir Mollaei; Maria Suarez-Diez; Vicente T Sedano-Nunez; Sjef Boeren; Alfons J M Stams; Caroline M Plugge

doi:10.3389/fmicb.2021.708911

Proteomic Analysis of a Syntrophic Coculture of Syntrophobacter fumaroxidans MPOB^T and Geobacter sulfurreducens PCA^T

Front Microbiol. 2021 Nov 30:12:708911. doi: 10.3389/fmicb.2021.708911. eCollection 2021.

Authors

Monir Mollaei^{1

2}, Maria Suarez-Diez³, Vicente T Sedano-Nunez², Sjef Boeren⁴, Alfons J M Stams^{2

5}, Caroline M Plugge^{1

2}

Affiliations

¹ Wetsus, European Centre of Excellence for Sustainable Water Technology, Leeuwarden, Netherlands.
² Laboratory of Microbiology, Wageningen University & Research, Wageningen, Netherlands.
³ Laboratory of Systems and Synthetic Biology, Wageningen University & Research, Wageningen, Netherlands.
⁴ Laboratory of Biochemistry, Wageningen University & Research, Wageningen, Netherlands.
⁵ Centre of Biological Engineering, University of Minho, Braga, Portugal.

Abstract

We established a syntrophic coculture of Syntrophobacter fumaroxidans MPOB^T (SF) and Geobacter sulfurreducens PCA^T (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.

Keywords: Geobacter sulfurreducens; Syntrophobacter fumaroxidans; coculture; interspecies electron transfer; propionate; proteomics.