Abstract

Shewanella oneidensis MR-1 can transfer electrons from the intracellular environment to the extracellular space of the cells to reduce the extracellular insoluble electron acceptors (Extracellular Electron Transfer, EET). Benefiting from this EET capability, Shewanella has been widely used in different areas, such as energy production, wastewater treatment, and bioremediation. Genome-wide proteomics data was used to determine the active proteins involved in activating the EET process. We identified 1012 proteins with decreased expression and 811 proteins with increased expression when the EET process changed from inactivation to activation. We then networked these proteins to construct the active protein networks, and identified the top 20 key active proteins by network centralization analysis, including metabolism- and energy-related proteins, signal and transcriptional regulatory proteins, translation-related proteins, and the EET-related proteins. We also constructed the integrated protein interaction and transcriptional regulatory networks for the active proteins, then found three exclusive active network motifs involved in activating the EET process—Bi-feedforward Loop, Regulatory Cascade with a Feedback, and Feedback with a Protein–Protein Interaction (PPI)—and identified the active proteins involved in these motifs. Both enrichment analysis and comparative analysis to the whole-genome data implicated the multiheme c-type cytochromes and multiple signal processing proteins involved in the process. Furthermore, the interactions of these motif-guided active proteins and the involved functional modules were discussed. Collectively, by using network-based methods, this work reported a proteome-wide search for the key active proteins that potentially activate the EET process.

Highlights

  • Shewanella oneidensis MR-1 is one of the most well-known electricigens, which can transfer the electrons produced inside of the cells to the outside of the cells to restore extracellular insoluble solid electron acceptors [1,2]

  • Since S3 was sampled from the last steady state under high-O2 conditions while S4 was sampled from the first steady state under low-O2 conditions, the severe changes between S3 and S4 should reflect the transition from high-O2

  • Total of proteins were found to be associated with the and functional modules has been carried out to identify the key active proteins capable of activating changed electron transfer (EET) process by clustering analysis. These active proteins were networked, and the top 20 key active proteins were identified by network centralization analysis; these proteins may serve as prospective targets for experimental confirmation

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Summary

Introduction

Shewanella oneidensis MR-1 is one of the most well-known electricigens, which can transfer the electrons produced inside of the cells to the outside of the cells to restore extracellular insoluble solid electron acceptors (extracellular electron transfer, EET) [1,2]. S. oneidensis MR-1 can extend its outer membrane to form electrically conductive bacterial nanowires for promoting the EET process under anaerobic conditions, and the c-type cytochromes that are contained in the surface of the outer membrane are known to play an important role in the EET process [5,6]. With the advances in high-throughput technologies, a large number of studies have been constructed to investigate the EET process in S. oneidensis MR-1 from genome-wide expression profiles. These studies used the differential expression information from RNA-level gene expression datasets that were derived from different EET conditions [7,8,9].

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