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Front. Microbiol. | doi: 10.3389/fmicb.2019.00003

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

 David C. Vuono1, 2*,  Robert W. Read1,  James Hemp3, Benjamin W. Sullivan4, John A. Arnone1, Iva Neveux1, Robert R. Blank5, Evan Loney1, David Miceli1,  Mari-Karoliina H. Winkler2,  Romy Chakraborty6,  David A. Stahl2 and  Joseph Grzymski1
  • 1Desert Research Institute (DRI), United States
  • 2University of Washington, United States
  • 3California Institute of Technology, United States
  • 4University of Nevada, Reno, United States
  • 5Agricultural Research Service, United States Department of Agriculture, United States
  • 6Lawrence Berkeley National Laboratory (LBNL), United States

Respiratory ammonification and denitrification are two evolutionarily unrelated dissimilatory nitrogen (N) processes central to the global N cycle, the activity of which is thought to be controlled by carbon (C) to nitrate (NO3-) ratio. Here we find that Intrasporangium calvum C5, a novel dual-pathway denitrifier/respiratory ammonifier, disproportionately utilizes ammonification rather than denitrification when grown under low C concentrations, even at low C:NO3- ratios. This finding is in conflict with the paradigm that high C:NO3- ratios promote ammonification and low C:NO3- ratios promote denitrification. We find that the protein atomic composition for denitrification modules (NirK) are significantly cost minimized for C and N compared to ammonification modules (NrfA), indicating that limitation for C and N is a major evolutionary selective pressure imprinted in the architecture of these proteins. The evolutionary precedent for these findings suggests ecological importance for microbial activity as evidenced by higher growth rates when I. calvum grows predominantly using its ammonification pathway and by assimilating its end-product (ammonium) for growth under ammonium-free conditions. Genomic analysis of I. calvum further reveals a versatile ecophysiology to cope with nutrient stress and redox conditions. Metabolite and transcriptional profiles during growth indicate that enzyme modules, NrfAH and NirK, are not constitutively expressed but rather induced by nitrite production via NarG. Mechanistically, our results suggest that pathway selection is driven by intracellular redox potential (redox poise), which may be lowered when resource concentrations are low, thereby decreasing catalytic activity of upstream electron transport steps (i.e., the bc1 complex) needed for denitrification enzymes. Our work advances our understanding of the biogeochemical flexibility of N-cycling organisms, pathway evolution, and ecological food-webs.

Keywords: Dissimilatory nitrate reduction, Denitrification, ammonification, Redox poise, Cost minimization, Maximum power principle

Received: 10 Oct 2018; Accepted: 07 Jan 2019.

Edited by:

Marina G. Kalyuzhanaya, San Diego State University, United States

Reviewed by:

Marc Strous, University of Calgary, Canada
Thomas E. Hanson, University of Delaware, United States  

Copyright: © 2019 Vuono, Read, Hemp, Sullivan, Arnone, Neveux, Blank, Loney, Miceli, Winkler, Chakraborty, Stahl and Grzymski. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. David C. Vuono, Desert Research Institute (DRI), Reno, United States, David.Vuono@dri.edu