Transcriptional regulatory module analysis reveals that bridge proteins reconcile multiple signals in extracellular electron transfer pathways

Abstract

Shewanella oneidensis MR‐1 shows remarkable respiratory versatility with a large variety of extracellular electron acceptors (termed extracellular electron transfer, EET). To utilize the various electron acceptors, the bacterium must employ complex regulatory mechanisms to elicit the relevant EET pathways. To investigate the relevant mechanisms, we integrated EET genes and related transcriptional factors (TFs) into transcriptional regulatory modules (TRMs) and showed that many bridge proteins in these modules were signal proteins, which generally contained one or more signal processing domains (eg, GGDEF, EAL, PAS, etc.). Since Shewanella has to respond to diverse environmental conditions despite encoding few EET‐relevant TFs, the overabundant signal proteins involved in the TRMs can help decipher the mechanism by which these microbes elicit a wide range of condition‐specific responses. By combining proteomic data and protein bioinformatic analysis, we demonstrated that diverse signal proteins reconciled the different EET pathways, and we discussed the functional roles of signal proteins involved in the well‐known MtrCAB pathway. Additionally, we showed that the signal proteins SO_2145 and SO_1417 played central roles in triggering EET pathways in anaerobic environments. Taken together, our results suggest that signal proteins have a profound impact on the transcriptional regulation of EET genes and thus have potential applications in microbial fuel cells.

Co-fitness analysis identifies a diversity of signal proteins involved in the utilization of specific c-type cytochromes

“…Further examination showed that there were 39 signal proteins in this 203-node co-fitness network, and the ratio (~19.2%; 39/203) of signal proteins was far higher than that of the Shewanella genome (~9.8%). These results are consistent with our previous studies on electron transfer pathways using transcriptional regulation modules (TRMs); that is, Shewanella needs a large number of signal transduction proteins to deal with its most important electron transfer process (Ding et al 2020).…”

“…Therefore, both molecular function and KEGG pathway analyses suggest the enrichment of signal transduction proteins in the co-fitness genes of c-type cytochromes. Although the complex regulatory mechanism and a lot of signal proteins involved in the EET process of Shewanella have been widely discussed (Fredrickson et al 2008;Rodionov et al 2011;Sundararajan et al 2011;Ding et al 2020), systematic study of signal proteins related to all c-type cytochrome in Shewanella has not been reported. These results can be further used to explain why a diverse set of c-type cytochromes is responsible for the diversity of Shewanella respiration, as well as how these c-type cytochromes are appropriately triggered under different conditions.…”