Tuning the modular Paracoccus denitrificans respirome to adapt from aerobic respiration to anaerobic denitrification

Abstract

Summary Bacterial denitrification is a respiratory process that is a major source and sink of the potent greenhouse gas nitrous oxide. Many denitrifying bacteria can adjust to life in both oxic and anoxic environments through differential expression of their respiromes in response to environmental signals such as oxygen, nitrate and nitric oxide. We used steady‐state oxic and anoxic chemostat cultures to demonstrate that the switch from aerobic to anaerobic metabolism is brought about by changes in the levels of expression of relatively few genes, but this is sufficient to adjust the configuration of the respirome to allow the organism to efficiently respire nitrate without the significant release of intermediates, such as nitrous oxide. The regulation of the denitrification respirome in strains deficient in the transcription factors FnrP, Nnr and NarR was explored and revealed that these have both inducer and repressor activities, possibly due to competitive binding at similar DNA binding sites. This may contribute to the fine tuning of expression of the denitrification respirome and so adds to the understanding of the regulation of nitrous oxide emission by denitrifying bacteria in response to different environmental signals.

Systems biology approaches towards predictive microbial ecology

“…In‐depth understanding of denitrification and nitrification pathways is mainly based on pure culture studies in the laboratory with model organisms, such as the denitrifier Paracoccus denitrificans. Through dozens of studies that employ a range of techniques (e.g., transcriptomics, proteomics, enzyme kinetics, gas flux analysis), its denitrification phenotype, including biochemical pathways and regulatory networks involved, has been well‐characterized (Bakken et al, ; Qu et al, ; Giannopoulos et al, ; Olaya‐Abril et al, ; Bergaust et al, ). For example, higher N 2 O production is associated with low pH conditions, an observation that is consistent with field observations (SImek & Cooper, ).…”

A dual functional redox enzyme maturation protein for respiratory and assimilatory nitrate reductases in bacteria

“…The P. denitrificans narKGHJI gene cluster is known to be expressed under anaerobic conditions during respiration and is regulated by the oxygen and / responsive transcription factors FnrP and NarR respectively (Wood et al , ), consistent with the key role of these genes in denitrification (Giannopoulos et al , ). By contrast, the nasABGHC genes are expressed in response to the C/N‐status of the cell and independently to oxygen tension when or is present (Gates et al , ; Luque‐Almagro et al , ).…”

Diversifying Anaerobic Respiration Strategies to Compete in the Rhizosphere

“…Nar is composed of 3 subunits encoded by narGHI, as found in E. coli, P. fluorescens, P. stutzeri and B. subtilis (Philippot and Højberg, 1999;Lalucat et al, 2006), whereas Nap is composed of 2 subunits encoded by napAB, as found in Rhodabacter sphaeroides and B. japonicum (Reyes et al, 1998;Bedmar et al, 2005). The nar operon is induced under low oxygen partial pressure and in the presence of nitrogen oxides (Philippot et al, 2001;Giannopoulos et al, 2017), whereas the expression of the nap operon can be affected or not by anaerobiosis depending on the organism (Philippot, 2002;Bueno et al, 2017).…”