Denitrification in low oxic environments increases the accumulation of nitrogen oxide intermediates and modulates the evolutionary potential of microbial populations

Author:

Takahashi Kohei12,Oshiki Mamoru3,Ruan Chujin2,Morinaga Kana2,Toyofuku Masanori45,Nomura Nobuhiko45,Johnson David R.26ORCID

Affiliation:

1. Graduate School of Sciences and Technologies University of Tsukuba Tsukuba Ibaraki Japan

2. Department of Environmental Microbiology Swiss Federal Institute of Aquatic Science and Technology (Eawag) Dübendorf Switzerland

3. Division of Environmental Engineering, Faculty of Engineering Hokkaido University Sapporo Hokkaido Japan

4. Faculty of Life and Environmental Sciences University of Tsukuba Tsukuba Ibaraki Japan

5. Microbiology Research Center for Sustainability University of Tsukuba Tsukuba Ibaraki Japan

6. Institute of Ecology and Evolution University of Bern Bern Switzerland

Abstract

AbstractDenitrification in oxic environments occurs when a microorganism uses nitrogen oxides as terminal electron acceptors even though oxygen is available. While this phenomenon is well‐established, its consequences on ecological and evolutionary processes remain poorly understood. We hypothesize here that denitrification in oxic environments can modify the accumulation profiles of nitrogen oxide intermediates with cascading effects on the evolutionary potentials of denitrifying microorganisms. To test this, we performed laboratory experiments with Paracoccus denitrificans and complemented them with individual‐based computational modelling. We found that denitrification in low oxic environments significantly increases the accumulation of nitrite and nitric oxide. We further found that the increased accumulation of these intermediates has a negative effect on growth at low pH. Finally, we found that the increased negative effect at low pH increases the number of individuals that contribute to surface‐associated growth. This increases the amount of genetic diversity that is preserved from the initial population, thus increasing the number of genetic targets for natural selection to act upon and resulting in higher evolutionary potentials. Together, our data highlight that denitrification in low oxic environments can affect the ecological processes and evolutionary potentials of denitrifying microorganisms by modifying the accumulation of nitrogen oxide intermediates.

Funder

Exploratory Research for Advanced Technology

Fusion Oriented REsearch for disruptive Science and Technology

Japan Society for the Promotion of Science

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung

Publisher

Wiley

Subject

Agricultural and Biological Sciences (miscellaneous),Ecology, Evolution, Behavior and Systematics

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