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Stimulation of Smithella‐dominating propionate oxidation in a sediment enrichment by magnetite and carbon nanotubes

Xia, Xingxuan, Zhang, Jianchao, Song, Tianze, Lu, Yahai
Environmental microbiology reports 2019 v.11 no.2 pp. 236-248
Methanosaeta, Methanosarcina, Smithella, Syntrophomonas, acetates, anaerobic digesters, biodegradation, butyrates, carbon nanotubes, electron transfer, enrichment culture, fluorescence in situ hybridization, formates, habitats, hydrogen, lakes, magnetite, methane, methane production, methanogens, organic matter, oxidation, population structure, propionic acid, scanning electron microscopes, sediments, short chain fatty acids, silica
Recent studies have shown that application of conductive materials including magnetite and carbon nanotubes (CNTs) can promote the methanogenic decomposition of short‐chain fatty acids and even more complex organic matter in anaerobic digesters and natural habitats. The linkage to microbial identity and the mechanisms, however, remain poorly understood. Here, we evaluate the effects of nanoscale magnetite (nanoFe₃O₄) and multiwalled CNTs on the syntrophic oxidation of propionate in an enrichment obtained from lake sediment. The microbial populations were composed mainly of Smithella, Syntrophomonas, Methanosaeta, Methanosarcina and Methanoregula. In addition to acetate, butyrate was transiently accumulated indicating that propionate was oxidized by Smithella via the dismutation pathway and part of the leaked butyrate was oxidized by Syntrophomonas. Propionate oxidation and CH₄ production were significantly accelerated in the presence of nanoFe₃O₄ and CNTs. While propionate oxidation was suppressed upon H₂ application and suspended completely upon formate application in the control, this suppressive effect was substantially compromised in the presence of nanoFe₃O₄ and CNTs. The tests on hydrogenotrophic methanogenesis of a pure culture methanogen and of the enrichment culture without propionate showed negative effect by both materials. The positive effect of nanoFe₃O₄ disappeared when it was insulated by surface‐coating with silica. Observations made with fluorescence in situ hybridization and scanning electron microscope indicated the extensive formation of microbial cell‐conductive material mixture aggregates. Our results suggest that direct interspecies electron transfer is likely activated by the conductive materials and operates in concert with H₂/formate‐dependent electron transfer for syntrophic propionate oxidation in the sediment enrichment.