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ISME J., May 14 2025, wraf092 | https://doi.org/10.1093/ismejo/wraf092 Hydrogen-dependent dissimilatory nitrate reduction to ammonium enables growth of Campylobacterota isolates

Hokwan Heo¹, Thanh Nguyen-Dinh², Man-Young Jung^3,4, Chris Greening², and Sukhwan Yoon^1,#

¹Department of Civil and Environmental Engineering, Korea Advanced Institute of Science and Technology (KAIST), Daejeon 34141, Republic of Korea
²Department of Microbiology, Biomedicine Discovery Institute, Monash University, Clayton, Victoria 3800, Australia.
³Interdisciplinary Graduate Program in Advance Convergence Technology and Science, Jeju National University, Jeju 63243, Republic of Korea
⁴Department of Biology Education, Jeju National University, Jeju 63243, Republic of Korea

^#Corresponding author: Sukhwan Yoon

Abstract

Dissimilatory nitrate reduction to ammonium (DNRA) is a key process used by diverse microorganisms in the global nitrogen cycle. For long, DNRA has been considered primarily as an organotrophic reaction, despite evidence that oxidation of inorganic electron donors also supports DNRA. Evidence of DNRA coupling with molecular hydrogen (H2) oxidation has been reported for several microbial isolates; however, the underlying physiology of the microbial process remains understudied. In this study, we report the isolation of two Campylobacterotastrains, Aliarcobacter butzlerihDNRA1 and Sulfurospirillumsp. hDNRA2, which grow using H2as the sole electron donor for DNRA, and physiological insights gained from a close examination of hydrogenotrophic DNRA in these isolates. In both batch and continuous cultures, DNRA sensu stricto(i.e. NO3-reduction that includes stoichiometric NO2--to-NH4+reduction) was strictly dependent on the presence of H2and exhibited stoichiometric coupling with H2oxidation, indicating that electrons required for NO2-reduction were unequivocally derived from H2. Successful chemostat incubation further demonstrated that hydrogenotrophic DNRA is viable under NO3-limiting, H2-excess conditions. Genomic and transcriptomic analyses identified group 1b [NiFe]-hydrogenase and cytochrome c552nitrite reductase as the key enzymes catalyzing hydrogenotrophic DNRA. Additionally, metagenomic surveys revealed that bacteria capable of hydrogenotrophic DNRA are taxonomically diverse and abundant in various ecosystems, particularly in the vicinity of deep-sea hydrothermal vents. These findings, integrating physiological, genomic, and transcriptomic analyses, clarify that H2can solely serve as a growth-supporting electron donor for DNRA and suggest potential significance of this microbial process in nitrogen- and hydrogen-related environmental biogeochemical cycles.

논문정보

형식Research article
게재일2025년 05월 (BRIC 등록일 2025-05-15)
연구진국내(교신)+국외 연구진
분야 생명과학 > 미생물학

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