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.
Highlights
Nitrogen is one of the building blocks of life and occurs naturally throughout the planet (Brandes et al, 2007; Denk et al, 2017; Kuypers et al, 2018)
Nitrate reduction in WP3 has been extensively studied under atmospheric pressure conditions, but its characteristics under high hydrostatic pressure (HHP) conditions close to its original habitat remain unknown
We demonstrated that two NAP systems have distinct responses to HHP at both the gene transcription level and enzyme activity level, suggesting different functions and contributions in nitrate reduction in the deep-sea environment
Summary
Nitrogen is one of the building blocks of life and occurs naturally throughout the planet (Brandes et al, 2007; Denk et al, 2017; Kuypers et al, 2018). It forms numerous compounds with different chemical valences, and chemical transformations among them constitute the network of global nitrogen biogeochemical cycles (Stein and Klotz, 2016). Being one of the most stable nitrogen compounds, nitrate can be retained in soils, sediments, and seawater (Sparacino-Watkins et al, 2014). The assimilatory nitrate reductase (Nas) is a soluble cytoplasmic protein that incorporates nitrogen from nitrate into the organism’s biomass (Kilic et al, 2017), while the membrane-bound (Nar) and the periplasmic (Nap) dissimilatory nitrate reductases (Nar and Nap) excrete the end products of nitrate reduction out of the cells
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