Resource Concentration Modulates the Fate of Dissimilated Nitrogen in a Dual-Pathway Actinobacterium

Vuono, David C.; Read, Robert W.; Hemp, James; Sullivan, Benjamin W.; Arnone III, John A.; Neveux, Iva; Blank, Robert R.; Loney, Evan; Miceli, David; Winkler, Mari-Karoliina H.; Chakraborty, Romy; Stahl, David A.; Grzymski, Joseph J.

doi:10.3389/fmicb.2019.00003

Title: Resource Concentration Modulates the Fate of Dissimilated Nitrogen in a Dual-Pathway Actinobacterium

Journal Article · Tue Jan 22 00:00:00 EST 2019 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2019.00003· OSTI ID:1560586

Vuono, David C. ^[1]; Read, Robert W. ^[2]; Hemp, James ^[3]; Sullivan, Benjamin W. ^[4]; Arnone III, John A. ^[2]; Neveux, Iva ^[2]; Blank, Robert R. ^[5]; Loney, Evan ^[2]; Miceli, David ^[2]; Winkler, Mari-Karoliina H. ^[6]; Chakraborty, Romy ^[7]; Stahl, David A. ^[6]; Grzymski, Joseph J. ^[2]

Desert Research Inst., Reno, NV (United States). Division of Earth and Ecosystem Sciences; Univ. of Washington, Seattle, WA (United States). Dept. of Civil and Environmental Engineering
Desert Research Inst., Reno, NV (United States). Division of Earth and Ecosystem Sciences
California Inst. of Technology, Pasadena, CA (United States)
Univ. of Nevada, Reno, NV (United States). Dept. of Natural Resources and Environmental Science
United States Dept. of Agriculture, Reno, NV (United States)
Univ. of Washington, Seattle, WA (United States). Dept. of Civil and Environmental Engineering
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; AC05-00OR22725

OSTI ID:: 1560586

Journal Information:: Frontiers in Microbiology, Vol. 10, Issue JAN; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 9 works

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Ecological and physiological implications of nitrogen oxide reduction pathways on greenhouse gas emissions in agroecosystems Yoon, Sukhwan; Song, Bongkeun; Phillips, Rebecca L. FEMS Microbiology Ecology, Vol. 95, Issue 6 https://doi.org/10.1093/femsec/fiz066	journal	May 2019
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59 BASIC BIOLOGICAL SCIENCES
dissimilatory nitrate reduction
denitrification
ammonification
redox poise
cost minimization
maximum power principle