Metabolic versatility of the nitrite-oxidizing bacterium Nitrospira marina and its proteomic response to oxygen-limited conditions

Abstract

<jats:title>Abstract</jats:title><jats:p>The genus <jats:italic>Nitrospira</jats:italic> is the most widespread group of chemolithoautotrophic nitrite-oxidizing bacteria that thrive in diverse natural and engineered ecosystems. <jats:italic>Nitrospira marina</jats:italic> Nb-295<jats:sup>T</jats:sup> represents the type genus and was isolated from the oceanic water column over 30 years ago, however, its genome has not yet been analyzed. Here, we analyzed the complete genome sequence of <jats:italic>N. marina</jats:italic> and performed select physiological experiments to test genome-derived hypotheses. Our data confirm that <jats:italic>N. marina</jats:italic> benefits from additions of undefined organic carbon substrates, has adaptations to combat oxidative, osmotic and UV-light induced stress and low dissolved <jats:italic>p</jats:italic>CO<jats:sub>2</jats:sub>, and is able to grow chemoorganotrophically on formate. We further investigated the metabolic response of <jats:italic>N. marina</jats:italic> to low (∼5.6 µM) O<jats:sub>2</jats:sub> concentrations commonly encountered in marine environments with high nitrite concentrations. In response to O<jats:sub>2</jats:sub>-limited conditions, the abundance of a potentially more efficient CO<jats:sub>2</jats:sub>-fixing pyruvate:ferredoxin oxidoreductase (POR) complex and a high affinity <jats:italic>cbb3</jats:italic>-type terminal oxidase increased, suggesting a role in sustaining nitrite oxidation-driven autotrophy under O<jats:sub>2</jats:sub> limitation. Additionally, a Cu/Zn-binding superoxide dismutase increased in abundance potentially protecting this putatively more O<jats:sub>2</jats:sub>-sensitive POR complex from oxidative damage. An increase in abundance of proteins involved in alternative energy metabolisms, including type 3b [NiFe] hydrogenase and formate dehydrogenase, indicate a high metabolic versatility to survive conditions unfavorable for aerobic nitrite oxidation. In summary, the genome and proteome of the first marine <jats:italic>Nitrospira</jats:italic> isolate identifies adaptations to life in the oxic ocean and provides important insights into the metabolic diversity and niche differentiation of NOB in marine environments.</jats:p>

Existence and distribution of novel phylotypes of Nitrospira in water columnsof the South China Sea

“…Nevertheless, N. marina-related species accounted for only 1.39% of nxrB sequences in the water columns of the SCS in our study. Although biosynthesis pathway in contrast to many other bacteria (Shelton et al, 2019;Bayer et al, 2021) and obtains VB 12 from the salvage of multiple intermediates from the environment (Bayer et al, 2021). Moreover, the salvage acquisition mode is closely correlated with organic ligands (B 12 precursors or degradation products), which is critical for dissolved cobalt speciation (Saito et al, 2005;Bayer et al, 2021).…”

“…Although B vitamins have an important role in cellular metabolism, N. marina lacks a complete vitamin B 12 (VB 12 ) biosynthesis pathway in contrast to many other bacteria ( Shelton et al., 2019 ; Bayer et al., 2021 ) and obtains VB 12 from the salvage of multiple intermediates from the environment ( Bayer et al., 2021 ). Moreover, the salvage acquisition mode is closely correlated with organic ligands (B 12 precursors or degradation products), which is critical for dissolved cobalt speciation ( Saito et al., 2005 ; Bayer et al., 2021 ). Interestingly, organic cobalt complexes are rich in the North Atlantic ocean, where N. marina was isolated ( Noble et al., 2017 ).…”

“…However, comammox bacteria have not been discovered in marine ecosystems ( Daims et al., 2015 ; Mao et al., 2020 ). Nitrification not only supplies nitrate as the primary source of biologically available nitrogen for assimilation by phytoplankton and microorganisms in surface water ( Gruber, 2018 ; Bayer et al., 2021 ) but also contributes markedly to carbon fixation in the dark ocean ( Pachiadaki et al., 2017 ; Zhang et al., 2020 ). It may also be a source of nitrous oxide for the atmosphere ( Prosser et al., 2020 ; Breider et al., 2019 ).…”