Metabolite-enabled mutualistic interaction between Shewanella oneidensis and Escherichia coli in a co-culture using an electrode as electron acceptor.

Victor Bochuan Wang,Qichun Zhang,Staffan Kjelleberg,Say Chye Joachim Loo,Bin Cao,Liang Yang,Krishnakumar Sivakumar

doi:10.1038/srep11222

Abstract

Mutualistic interactions in planktonic microbial communities have been extensively studied. However, our understanding on mutualistic communities consisting of co-existing planktonic cells and biofilms is limited. Here, we report a planktonic cells-biofilm mutualistic system established by the fermentative bacterium Escherichia coli and the dissimilatory metal-reducing bacterium Shewanella oneidensis in a bioelectrochemical device, where planktonic cells in the anode media interact with the biofilms on the electrode. Our results show that the transfer of formate is the key mechanism in this mutualistic system. More importantly, we demonstrate that the relative distribution of E. coli and S. oneidensis in the liquid media and biofilm is likely driven by their metabolic functions towards an optimum communal metabolism in the bioelectrochemical device. RNA sequencing-based transcriptomic analyses of the interacting organisms in the mutualistic system potentially reveal differential expression of genes involved in extracellular electron transfer pathways in both species in the planktonic cultures and biofilms.

Highlights

Mutualistic interactions in planktonic microbial communities have been extensively studied
Escherichia coli was chosen as a representative fermentative microorganism as it is easy to culture with simple nutritional requirements and its genome sequence is relatively well annotated[8], while S. oneidensis, a well-studied metal-reducing bacterium capable of reducing a wide range of metal ions, was used as a model anaerobically respiring bacteria
To test the mutualistic co-culture relationship between wild type E. coli and S. oneidensis strains, microbial fuel cells (MFCs) were employed as a platform to determine the extent of extracellular electron transfer in terms of electrical output in bioelectrochemical devices, with both species inoculated into the anode chamber

Summary

Results and Discussion

It is noteworthy to mention that the electrode serves as the sole electron acceptor for S. oneidensis respiration while the only carbon source (glucose) for E. coli fermentation is in the aqueous media This observation implies that the distribution of each species in the mutualistic community could be driven by metabolic functions towards an optimum communal metabolism (Fig. 4a,b). Expression of genes involved in the MTR pathway (cymA, mtrA, mtrC, omcA and mtrB) and flavin biosynthesis (fccA, frdA, SO 3468 and ribE) are notably increased These observations suggest a likely advantage for S. oneidensis biofilms to preferentially form on the electrode surface as it beneficially contributes to the communal interactions between both species in the area of charge transfer. This study reports a function-driven structural assembly of mutualistic communities consisting of planktonic cells interacting with biofilms

Methods

Formate dehydrogenase genes Function

Biofilms on electrode in anode chamber Function

Additional Information