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Resource limitation modulates the fate of dissimilated nitrogen in a dual-pathway Actinobacterium

By David C. Vuono, Robert W. Read, James Hemp, Benjamin W Sullivan, John A Arnone, Iva Neveux, Bob Blank, Carl Staub, Evan Loney, David Miceli, Mari Winkler, Romy Chakraborty, David A. Stahl, Joseph J Grzymski

Posted 08 Jul 2018
bioRxiv DOI: 10.1101/364331

Carbon to nitrate (C:NO3-) ratios are thought to modulate pathway selection between respiratory ammonification and denitrification, two nitrogen (N) dissimilatory processes vital to the global N budget. However, the molecular mechanisms that enable the selection of these pathways remains unclear. Here we evaluate C:NO3- control on pathway selection in Intrasporangium calvum C5, a Gram-positive menaquinone-based dual-pathway denitrifier/respiratory ammonifier and show that C:NO3- control theory is insufficient to explain pathways selection. We demonstrate that the bacterium disproportionately utilizes ammonification rather than denitrification (with nitrous oxide as its terminal end-product) when grown under carbon or nitrate limitation, not C:NO3- ratio. The ammonification pathway also promoted higher bacterial growth rates. Time series analysis of metabolite and transcriptional profiles during growth showed that transcript abundances for nitrite reducing complexes, NrfAH and NirK, significantly increased in response to nitrite production. Although lactate was the only carbon source provided to the organism, we detected formate production during growth (~200 μM), a five-fold upregulation in formate transporters, and a simultaneous up-regulation of formate dehydrogenase used to translocate protons via a quinol-loop. These results suggest that additional reducing equivalents can be obtained from a single carbon source and used for ammonification during resource limitation. Mechanistically, pathway selection may be driven by intracellular redox potential (redox poise), which is lowered during resource limitation, thereby decreasing catalytic activity of the bc1 complex (an upstream electron transport step needed for denitrification). Our work advances our understanding of the conditions and underlying mechanisms that select for denitrification and respiratory ammonification in environmental systems.

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