Wide distribution of extracellular electron transfer functionality in natural proteinaceous organic materials for microbial reductive dehalogenation

• Published in: Journal of bioscience and bioengineering 2023-03, Vol.135 (3), p.238-249
• Main Authors: Hu, Tingting, Yamaura, Mirai, Pham, Duyen Minh, Kasai, Takuya, Katayama, Arata
• Format: Article
• Language: English
• Subjects: Electron Transport; Electrons; Extracellular electron transfer materials; Humic Substances - analysis; Natural organic materials; PCP dechlorination; Pentachlorophenol - metabolism; Protein secondary structure; Reduced sulfur; Spectrum Analysis; β-sheet
• ISSN: 1389-1723; 1347-4421
• DOI: 10.1016/j.jbiosc.2022.12.003

Extracellular electron transfer materials (EETMs) in the environment, such as humic substances and biochar, are formed from the humification/heating of natural organic materials. However, the distribution of extracellular electron transfer (EET) functionality in fresh natural organic materials has not yet been explored. In the present study, we reveal the wide distribution of EET functionality in proteinaceous materials for the first time using an anaerobic pentachlorophenol dechlorinating consortium, whose activity depends on EETM. Out of 11 natural organic materials and 13 reference compounds, seven proteinaceous organic materials (albumin, beef, milk, pork, soybean, yolk, and bovine serum albumin) functioned as EETMs. Carbohydrates and lipids did not function as EETMs. Comparative spectroscopic analyses suggested that a β-sheet secondary structure was essential for proteins to function as EETMs, regardless of water solubility. A high content of reduced sulfur was potentially involved in EET functionality. Although proteinaceous materials have thus far been considered simply as nutrients, the wide distribution of EET functionality in these materials provides new insights into their impact on biogeochemical cycles. In addition, structural information on EET functionality can provide a scientific basis for the development of eco-friendly EETMs. [Display omitted] •Natural proteinaceous materials had extracellular electron transfer (EET) function.•The β-sheet secondary structure of proteins was crucial for the EET function.•A high content of reduced sulfur was potentially involved in the EET function.•Wide distribution of natural EET materials impacts biogeochemical cycling.•Structural information paves the synthetic study of eco-friendly EET materials.