Background and aims Microbial-driven dissimilatory nitrate reduction to ammonium (DNRA) is a unique pathway in the terrestrial nitrogen (N) cycle. It helps to retain N within the soil, preventing its loss to the surrounding environment. Due to the frequent flooding and draining, rice ecosystems experience both aerobic and anaerobic conditions, causing a shift in microbial process. Our goal in the present study was to understand the influence of various environmental factors and their regulatory mechanisms of DNRA pathway and also assess the nrfA gene-targeted (marker functional gene of DNRA) microbial community under diverse upland and lowland rice agro-ecosystems in sub-humid tropical condition. Methods Investigated rice agro-ecosystems for the present study were i) irrigated (IR), ii) three lowland, based on water depth i.e., shallow lowland: 0–30 cm; intermediate lowland: 30–50 cm; semi-deep lowland: 50–100 cm, and iii) two upland (dry or rainfed and aerobic) conditions. Soil physico-chemical and extracellular enzymatic activities, microbial dynamics and metabolism, nrfA-gene targeted metagenome, and both absolute and expressional quantification of nrfA-gene were performed and analysed under these diverse rice agro-ecosystems. Results Our findings showed that the DNRA activity was significantly (p < 0.05) correlated with the C/N ratio in arable paddy soil, which suggested that DNRA activity might be possible in diverse rice agro-ecosystems apart of anoxic reducing conditions. Biolog ecoplate-based study revealed that among different carbon guilds, amino acids utilising microbial community was more in semi-deep lowland compared to other rice agro-ecosystems. Interestingly, a higher (~ 20.44%) abundance of nrfA gene (7.01 log copy number g−1 soil) was found in semi-deep lowland compared to upland dry conditions. Similarly, the functional expression of nrfA transcripts copy number was found higher in semi-deep lowland, possibly due to the presence of predominant taxa belonged to class Deinococci and Anaerolineae. Conclusion Higher abundance of DNRA microbial communities such as Actinomyces radicidentis, Geobacter uraniireducens, Thermogutta terrifontis in lowland rice, and Anaeromyxobacter dehalogenase, and Anaeromyxobacter sp. Fw109-5 in upland rice conditions could suggest the adaptability and functionality of these microbial communities in response to diverse rice agro-ecosystems. Moreover, environmental conditions in paddy soils might be crucial for driving the DNRA pathway, and it is necessary to examine this adaptation from the perspective of microbial genome mining in order to clarify the ecological significance of DNRA in rice agro-ecosystems. Graphical abstract The schematic representation showed the terrestrial nitrogen cycle and mainly focused on dissimilatory nitrate reduction to ammonium (DNRA) pathway under i) irrigated (IR), ii) three lowland based on water depth i.e., shallow (SL): 0-30 cm; intermediate (IL): 30-50 cm; semi-deep (SD): 50-100 cm, and iii) two upland (dry or rainfed: DR and aerobic: AR) rice agro-ecosystems. This study quantified the functional gene abundance and expression of the DNRA process i.e., nrfA gene, under diverse rice agro-ecosystems. The nrfA-targeted bacterial community through the metagenome identified keystone DNRA bacterial taxa, the role of various edaphic factors, and their influence on the DNRA pathway under different upland and lowland sub-tropical rice agro-ecosystems.

Uncovering microbial drivers and regulatory edaphic factors for DNRA-nitrogen recovery under diverse rice agro-ecosystems

期刊论文
发表日期：

2025年1月31日

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Megha Kaviraj,
Upendra Kumar,
S. N. Chatterjee,
M. Shahid,
A. K. Nayak

摘要

Background and aims

Microbial-driven dissimilatory nitrate reduction to ammonium (DNRA) is a unique pathway in the terrestrial nitrogen (N) cycle. It helps to retain N within the soil, preventing its loss to the surrounding environment. Due to the frequent flooding and draining, rice ecosystems experience both aerobic and anaerobic conditions, causing a shift in microbial process. Our goal in the present study was to understand the influence of various environmental factors and their regulatory mechanisms of DNRA pathway and also assess the nrfA gene-targeted (marker functional gene of DNRA) microbial community under diverse upland and lowland rice agro-ecosystems in sub-humid tropical condition.

Methods

Investigated rice agro-ecosystems for the present study were i) irrigated (IR), ii) three lowland, based on water depth i.e., shallow lowland: 0–30 cm; intermediate lowland: 30–50 cm; semi-deep lowland: 50–100 cm, and iii) two upland (dry or rainfed and aerobic) conditions. Soil physico-chemical and extracellular enzymatic activities, microbial dynamics and metabolism, nrfA-gene targeted metagenome, and both absolute and expressional quantification of nrfA-gene were performed and analysed under these diverse rice agro-ecosystems.

Results

Our findings showed that the DNRA activity was significantly (p < 0.05) correlated with the C/N ratio in arable paddy soil, which suggested that DNRA activity might be possible in diverse rice agro-ecosystems apart of anoxic reducing conditions. Biolog ecoplate-based study revealed that among different carbon guilds, amino acids utilising microbial community was more in semi-deep lowland compared to other rice agro-ecosystems. Interestingly, a higher (~ 20.44%) abundance of nrfA gene (7.01 log copy number g⁻¹ soil) was found in semi-deep lowland compared to upland dry conditions. Similarly, the functional expression of nrfA transcripts copy number was found higher in semi-deep lowland, possibly due to the presence of predominant taxa belonged to class Deinococci and Anaerolineae.

Conclusion

Higher abundance of DNRA microbial communities such as Actinomyces radicidentis, Geobacter uraniireducens, Thermogutta terrifontis in lowland rice, and Anaeromyxobacter dehalogenase, and Anaeromyxobacter sp. Fw109-5 in upland rice conditions could suggest the adaptability and functionality of these microbial communities in response to diverse rice agro-ecosystems. Moreover, environmental conditions in paddy soils might be crucial for driving the DNRA pathway, and it is necessary to examine this adaptation from the perspective of microbial genome mining in order to clarify the ecological significance of DNRA in rice agro-ecosystems.

Graphical abstract

The schematic representation showed the terrestrial nitrogen cycle and mainly focused on dissimilatory nitrate reduction to ammonium (DNRA) pathway under i) irrigated (IR), ii) three lowland based on water depth i.e., shallow (SL): 0-30 cm; intermediate (IL): 30-50 cm; semi-deep (SD): 50-100 cm, and iii) two upland (dry or rainfed: DR and aerobic: AR) rice agro-ecosystems. This study quantified the functional gene abundance and expression of the DNRA process i.e., nrfA gene, under diverse rice agro-ecosystems. The nrfA-targeted bacterial community through the metagenome identified keystone DNRA bacterial taxa, the role of various edaphic factors, and their influence on the DNRA pathway under different upland and lowland sub-tropical rice agro-ecosystems.