Promoting bidirectional extracellular electron transfer of Shewanella oneidensis MR‐1 for hexavalent chromium reduction via elevating intracellular cAMP level

Abstract

The bioreduction capacity of Cr(VI) by Shewanella is mainly governed by its bidirectional extracellular electron transfer (EET). However, the low bidirectional EET efficiency restricts its wider applications in remediation of the environments contaminated by Cr(VI). Cyclic adenosine 3′,5′‐monophosphate (cAMP) commonly exists in Shewanella strains and cAMP–cyclic adenosine 3′,5′‐monophosphate receptor protein (CRP) system regulates multiple bidirectional EET‐related pathways. This inspires us to strengthen the bidirectional EET through elevating the intracellular cAMP level in Shewanella strains. In this study, an exogenous gene encoding adenylate cyclase from the soil bacterium Beggiatoa sp. PS is functionally expressed in Shewanella oneidensis MR‐1 (the strain MR‐1/pbPAC) and a MR‐1 mutant lacking all endogenous adenylate cyclase encoding genes (the strain Δca/pbPAC). The engineered strains exhibit the enhanced bidirectional EET capacities in microbial electrochemical systems compared with their counterparts. Meanwhile, a three times more rapid reduction rate of Cr(VI) is achieved by the strain MR‐1/pbPAC than the control in batch experiments. Furthermore, a higher Cr(VI) reduction efficiency is also achieved by the strain MR‐1/pbPAC in the Cr(VI)‐reducing biocathode experiments. Such a bidirectional enhancement is attributed to the improved production of cAMP–CRP complex, which upregulates the expression levels of the genes encoding the c‐type cytochromes and flavins synthetic pathways. Specially, this strategy could be used as a broad‐spectrum approach for the other Shewanella strains. Our results demonstrate that elevating the intracellular cAMP levels could be an efficient strategy to enhance the bidirectional EET of Shewanella strains and improve their pollutant transformation capacity.

Chemical-Assisted Microbially Mediated Chromium (Cr) (VI) Reduction Under the Influence of Various Electron Donors, Redox Mediators, and Other Additives: An Outlook on Enhanced Cr(VI) Removal

“…Adenylate cyclase expressing S. oneidensis MR−1 exhibited enhanced bidirectional EET and Cr(VI) reduction capacities. This was attributed to increased production of cyclic adenosine 3 ,5 −monophosphate (cAMP) and cAMP-receptor protein system, which enhanced the gene expression of c−type cytochromes and flavins synthetic pathways for Cr(VI) reduction (Cheng et al, 2020). Similarly, the outer membranes of Geobacter spp.…”

Biofilm Biology and Engineering of Geobacter and Shewanella spp. for Energy Applications

“…Briefly, several LuxR homologous genes are predicted in the genomes of Shewanella spp. including S. woodyi MS32 and S. baltica (Li J. et al, 2020;Hayek et al, 2020). The genome of S. oneidensis is predicted to contain seven putative LuxR family proteins.…”

“…The presence of both IPTG and AHL activates MtrA expression, which restores the EET pathway and increases electricity output (Hu et al, 2015). In another study, the lux QS system was used to construct a population-state decision system for intelligently reprogramming the EET regulation system (Li F.-H. et al, 2020). The EET-related genes or pathways, such as cymA, shuttle exporter genes or flavin biosynthesis pathway, were located at the downstream of QS system and could be expressed at a certain population-state threshold.…”

Promoting Extracellular Electron Transfer of Shewanella oneidensis MR-1 by Optimizing the Periplasmic Cytochrome c Network

“…In particular, by replacing with CctA a few terminal reductases, including NrfA, FccA, and NapA (periplasmic nitrate reductase), Delgado et al (2019) observed significantly increased ferric iron reduction rate and current generation. In addition, enhanced production of a large portion of c-Cyts by elevated cAMP levels, the effector molecule for Crp which is the primary transcriptional activator for anaerobic respiration, has also been found to be effective (Kasai et al, 2019;Cheng et al, 2020).…”