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

Vuono, David C. and Read, Robert W. and Hemp, James and Sullivan, Benjamin W. and Arnone, John A., III and Neveux, Iva and Blank, Bob and Staub, Carl and Loney, Evan and Miceli, David and Winkler, Mari and Chakraborty, Romy and Stahl, David A. and Grzymski, Joseph J. (2018) Resource limitation modulates the fate of dissimilated nitrogen in a dual-pathway Actinobacterium. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20200117-133400483

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Abstract

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 menaquinone-based dual-pathway denitrifier/respiratory ammonifier, disproportionately utilizes ammonification rather than denitrification when grown under carbon or nitrate limitation, not C:NO3- ratio. Instead, C:NO₃⁻ ratio is a confounding variable for resource limitation. 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 resource limitation is a major selective pressure imprinted in the architecture of these proteins. The evolutionary precedent for these findings suggests ecological and biogeochemical importance 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-deplete 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 transcript abundances encoding for its nitrite reducing enzyme modules, NrfAH and NirK, significantly increase in response to nitrite production. Mechanistically, our results suggest that pathway selection is driven by intracellular redox potential (redox poise), which may be lowered during resource limitation, thereby decreasing catalytic activity of upstream electron transport steps needed for denitrification enzymes. Our work advances our understanding of the biogeochemical flexibility of N-cycling organisms, pathway evolution, and ecological food-webs.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/364331DOIDiscussion Paper
ORCID:
AuthorORCID
Hemp, James0000-0001-7193-0553
Additional Information:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. bioRxiv preprint first posted online Jul. 8, 2018. We thank F. von Netzer, K. Hunt, S Morales, N. Stopnisek, K. Meinhardt, W. Qin, N Elliot, T. Hazen, H. Carlson, B. Ramsey, A. Murray, Z. Harrold, T. Morgan, and P. Longley for thoughtful feedback and discussions. This research was supported by a grant from the Nevada Governor’s Office of Economic Development (JG), by the Desert Research Institute (DRI) postdoctoral research fellowship program, and in part by Ecosystems and Networks Integrated with Genes and Molecular Assemblies (ENIGMA) (http://enigma.lbl.gov)—a Scientific Focus Area Program at Lawrence Berkeley National Laboratory under contract number DE-AC02-05CH11231 and funded in part by Oak Ridge National Laboratory under contract DE-AC05-00OR22725, and is based upon work supported by the U.S. Department of Energy, Office of Science, Office of Biological & Environmental Research. The authors declare no conflicts of interest.
Funders:
Funding AgencyGrant Number
Nevada Office of Economic DevelopmentUNSPECIFIED
Desert Research Institute (DRI)UNSPECIFIED
Ecosystems and Networks Integrated with Genes and Molecular Assemblies (ENIGMA)UNSPECIFIED
Department of Energy (DOE)DE-AC02-05CH11231
Department of Energy (DOE)DE-AC05-00OR22725
Record Number:CaltechAUTHORS:20200117-133400483
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200117-133400483
Official Citation:Resource limitation modulates the fate of dissimilated nitrogen in a dual-pathway Actinobacterium. David C. Vuono, Robert W. Read, James Hemp, Benjamin W. Sullivan, John A. Arnone III, Iva Neveux, Bob Blank, Carl Staub, Evan Loney, David Miceli, Mari Winkler, Romy Chakraborty, David A. Stahl, Joseph J. Grzymski. bioRxiv 364331; doi: https://doi.org/10.1101/364331
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:100798
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:17 Jan 2020 21:58
Last Modified:17 Jan 2020 21:58

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