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Resource Concentration 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, Robert R. and Loney, Evan and Miceli, David and Winkler, Mari-Karoliina H. and Chakraborty, Romy and Stahl, David A. and Grzymski, Joseph J. (2019) Resource Concentration Modulates the Fate of Dissimilated Nitrogen in a Dual-Pathway Actinobacterium. Frontiers in Microbiology, 10 . Art. No. 3. ISSN 1664-302X. PMCID PMC6349771. http://resolver.caltech.edu/CaltechAUTHORS:20180927-114224595

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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 (NO_3^−) 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:NO_3^− ratios. This finding is in conflict with the paradigm that high C:NO_3^− ratios promote ammonification and low C:NO_3^− 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. calvumfurther 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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.3389/fmicb.2019.00003DOIArticle
https://doi.org/10.1101/364331DOIDiscussion Paper
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6349771/PubMed CentralArticle
Alternate Title:Resource limitation modulates the fate of dissimilated nitrogen in a dual-pathway Actinobacterium
Additional Information:© 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. Received: 10 October 2018; Accepted: 07 January 2019; Published: 22 January 2019. We thank F. von Netzer, K. Hunt, S Morales, N. Stopnisek, K. Meinhardt, W. Qin, N Elliot, T. Hazen, H. Carlson, E. van den Berg, B. Ramsey, A. Murray, Z. Harrold, T. Morgan, R. Hallnan, and P. Longley for thoughtful feedback and discussions. A preprint version of this manuscript can be found on the preprint server bioRxiv (Vuono et al., 2018). Author Contributions: DV wrote the manuscript. DV, RR, M-KW, RC, DS, and JG contributed to the conception and designed the study. DV, BS, IN, RB, EL, and DM performed the lab work. DV, RR, JH, BS, JA, RB, M-KW, DS, and JG analyzed the data and interpreted the results. All authors contributed to manuscript revision, read, and approved the submitted version. 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 in part by Oak Ridge National Laboratory under contract DE-AC05-00OR22725, funded by the United States Department of Energy, Office of Science, Office of Biological and Environmental Research. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Funders:
Funding AgencyGrant Number
Nevada Office of Economic DevelopmentUNSPECIFIED
Ecosystems and Networks Integrated with Genes and Molecular Assemblies (ENIGMA)UNSPECIFIED
Desert Research InstituteUNSPECIFIED
Department of Energy (DOE)DE-AC02-05CH11231
Department of Energy (DOE) DE-AC05-00OR22725
Subject Keywords:dissimilatory nitrate reduction, denitrification, ammonification, redox poise, cost minimization, maximum power principle
PubMed Central ID:PMC6349771
Record Number:CaltechAUTHORS:20180927-114224595
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20180927-114224595
Official Citation:Vuono DC, Read RW, Hemp J, Sullivan BW, Arnone JA III, Neveux I, Blank RR, Loney E, Miceli D, Winkler M-KH, Chakraborty R, Stahl DA and Grzymski JJ (2019) Resource Concentration Modulates the Fate of Dissimilated Nitrogen in a Dual-Pathway Actinobacterium. Front. Microbiol. 10:3. doi: 10.3389/fmicb.2019.00003
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:90007
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:27 Sep 2018 21:10
Last Modified:07 Feb 2019 20:43

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