Pressure-Regulated Gene Expression and Enzymatic Activity of the Two Periplasmic Nitrate Reductases in the Deep-Sea Bacterium Shewanella piezotolerans WP3

Abstract

Shewanella species are widely distributed in marine environments, from the shallow coasts to the deepest sea bottom. Most Shewanella species possess two isoforms of periplasmic nitrate reductases (NAP-α and NAP-β) and are able to generate energy through nitrate reduction. However, the contributions of the two NAP systems to bacterial deep-sea adaptation remain unclear. In this study, we found that the deep-sea denitrifier Shewanella piezotolerans WP3 was capable of performing nitrate respiration under high hydrostatic pressure (HHP) conditions. In the wild-type strain, NAP-β played a dominant role and was induced by both the substrate and an elevated pressure, whereas NAP-α was constitutively expressed at a relatively lower level. Genetic studies showed that each NAP system alone was sufficient to fully sustain nitrate-dependent growth and that both NAP systems exhibited substrate and pressure inducible expression patterns when the other set was absent. Biochemical assays further demonstrated that NAP-α had a higher tolerance to elevated pressure. Collectively, we report for the first time the distinct properties and contributions of the two NAP systems to nitrate reduction under different pressure conditions. The results will shed light on the mechanisms of bacterial HHP adaptation and nitrogen cycling in the deep-sea environment.

Microbial communities reveal niche partitioning across the slope and bottom zones of the challenger deep

“…Similar to nitrogen cycling, abundant and distinct sulphate and sulphite reduction genes were observed between the slope and bottom. Nitrate and sulphate are common electron acceptors that follow oxygen, and their reduction was reported to be enhanced under high pressure (Li et al, 2018 ). Compared with aerobic respiration, anaerobic respiration processes, such as nitrate reduction, may reduce the production of ROS, and microbes may prefer nitrate as an electronic accepter instead of O 2 under HHP conditions.…”

Earthworms enhance the inhibition efficiency of 3,4-dimethylpyrazole phosphate on soil nitrification by altering soil AOB communities and gut denitrifier communities

“…6). This could be explained by the fact that all the three most abundant genera affiliated with Gammaproteobacteria (e.g., Aeromonas, Shewanella, and Citrobacter) have been previously identified as nitrifiers or denitrifiers (Chen et al 2014;Hau and Gralnick 2007;Huang and Tseng 2001;Li et al 2018;Tan et al 2020). However, all these genera could be significantly suppressed by DMPP application, which in turn, resulted in relatively higher microbial diversities and C-and P-cycling abilities of earthworm gut microbiota (Figs.…”

Comparative genomic analysis of obligately piezophilic Moritella yayanosii DB21MT-5 reveals bacterial adaptation to the Challenger Deep, Mariana Trench

“…Energy metabolism is one of the biological processes most susceptible to HHP. Possessing multiple cognate respiratory terminal oxido-reductases with different pressure tolerance and pressure-regulated electron transfer chain have been reported in diverse deep-sea microbes [56][57][58]. For example, in piezophilic Shewanella strain DB172F, the electron transfer chain utilized under atmospheric pressure is composed of bc1 complex, cytochrome c-551 and c-552 and cytochrome c oxidase, whereas the one under high pressure condition consists of cytochrome c-551 and quinol oxidase [59].…”