Biological nitrification inhibition in the rhizosphere: determining interactions and impact on microbially mediated processes and potential applications

Nardi, Pierfrancesco; Laanbroek, Hendrikus J.; Nicol, Graeme W.; Renella, Giancarlo; Cardinale, Massimiliano; Pietramellara, Giacomo; Weckwerth, Wolfram; Trinchera, Alessandra; Ghatak, Arindam; Nannipieri, Paolo

doi:10.1093/femsre/fuaa037

Cited by 96 publications

(71 citation statements)

References 468 publications

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“…This assumption aligns with the ongoing controversy on the ecological reasons for reduced net nitrification in certain climax ecosystems, i.e. grasslands and coniferous forests (Davidson et al 1992;Nardi et al 2020;Vazquez et al 2020). Precisely, it reflects our second hypothesis whether reduced net nitrification rates can be attributed to a BNI-induced reduction of gross nitrification rates.…”

Section: Tablesupporting

confidence: 67%

Inter-microbial competition for N and plant NO3− uptake rather than BNI determines soil net nitrification under intensively managed Brachiaria humidicola

et al. 2021

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Brachiaria humidicola (syn. Urochloa humidicola) has been acknowledged to control soil nitrification through release of nitrification inhibitors (NI), a phenomenon conceptualized as biological nitrification inhibition (BNI). Liming and N fertilization as features of agricultural intensification may suppress BNI performance, due to a decrease in NI exudation, increased NH3 availability and promotion of ammonia oxidizing bacteria (AOB) over archaea (AOA). A 2-year three-factorial pot trial was conducted to investigate the influence of soil pH and soil microbial background (ratio of archaea to bacteria) on BNI performance of B. humidicola. The study verified the capacity of B. humidicola to reduce net nitrification rates by 50 to 85% compared to the non-planted control, irrespective of soil pH and microbial background. The reduction of net nitrification, however, was largely dependent on microbial N immobilization and efficient plant N uptake. A reduction of gross nitrification could not be confirmed for the AOA dominated soil, but possibly contributed to reduced net nitrification rates in the AOB-dominated soil. However, this putative reduction of gross nitrification was attributed to plant-facilitated inter-microbial competition between bacterial heterotrophs and nitrifiers rather than BNI. It was concluded that BNI may play a dominant role in extensive B. humidicola pasture systems, while N immobilization and efficient plant N uptake may display the dominant factors controlling net nitrification rates under intensively managed B. humidicola.

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Section: Tablesupporting

confidence: 67%

Inter-microbial competition for N and plant NO3− uptake rather than BNI determines soil net nitrification under intensively managed Brachiaria humidicola

et al. 2021

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“…Fig. 2 UV-HPLC results: a relative abundance of the compounds identified in root exudate including phenolic acids; b relative abundance of the compounds identified in root exudate excluding phenolic acids (n:4, error bar = confidence interval 95%) the ability to manipulate the soil microbiome composition and biochemical activities, especially nitrification activity by biological nitrification inhibition (BNI), to improve the N use efficiency of the plant (Nardi et al 2020;Subbarao and Searchinger 2021). There is not much knowledge of how stress affects root exudation and plant-soil interactions.…”

Section: Genotypes Genotypesmentioning

confidence: 99%

Root exudation of contrasting drought-stressed pearl millet genotypes conveys varying biological nitrification inhibition (BNI) activity

et al. 2021

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Roots secrete a vast array of low molecular weight compounds into the soil broadly referred to as root exudates. It is a key mechanism by which plants and soil microbes interact in the rhizosphere. The effect of drought stress on the exudation process and composition is rarely studied, especially in cereal crops. This study focuses on comparative metabolic profiling of the exudates from sensitive and tolerant genotypes of pearl millet after a period of drought stress. We employed a combined platform of gas and liquid chromatography coupled to mass spectrometry to cover both primary and secondary metabolites. The results obtained demonstrate that both genotype and drought stress have a significant impact on the concentration and composition of root exudates. The complexity and function of these differential root exudates are discussed. To reveal the potential effect of root exudates on the soil microbial community after a period of drought stress, we also tested for biological nitrification inhibition (BNI) activity. The analysis revealed a genotype-dependent enhancement of BNI activity after a defined period of drought stress. In parallel, we observed a genotype-specific relation of elongated root growth and root exudation under drought stress. These data suggest that the drought stress-dependent change in root exudation can manipulate the microbial soil communities to adapt and survive under harsh conditions.

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“…The inhibitory effect does not last more than a few weeks, they have biologically limited stability, and SNI mobility could prevent these molecules from acting on the sites of nitrification [15,28]. On the other hand, BNIs are exuded directly into the rhizosphere, which is the main site of nitrification due to the great abundance of AOB and AOA [29]. Moreover, sorghum BNIs are known for being stable across a wide range of soil pH and temperature [14].…”

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confidence: 99%

Biological and synthetic approaches to inhibiting nitrification in non-tilled Mediterranean soils

Bozal-Leorri

Corrochano-Monsalve

Arregui

et al. 2021

Chem. Biol. Technol. Agric.

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Background The increasing demand for food production has led to a tenfold increase in nitrogen (N) fertilizer use since the Green Revolution. Nowadays, agricultural soils have been turned into high-nitrifying environments that increase N pollution. To decrease N losses, synthetic nitrification inhibitors (SNIs) such as 3,4-dimethylpyrazole phosphate (DMPP) have been developed. However, SNIs are not widely adopted by farmers due to their biologically limited stability and soil mobility. On the other hand, allelopathic substances from root exudates from crops such as sorghum are known for their activity as biological nitrification inhibitors (BNIs). These substances are released directly into the rhizosphere. Nevertheless, BNI exudation could be modified or even suppressed if crop development is affected. In this work, we compare the performance of biological (sorghum crop) and synthetic (DMPP) nitrification inhibitors in field conditions. Results Sorghum crop BNIs and DMPP prevented an increase in the abundance of ammonia-oxidizing bacteria (AOB) without affecting the total bacterial abundance. Both nitrification inhibitors maintained similar soil NH4+ content, but at 30 days post-fertilization (DPF), the sorghum BNIs resulted in higher soil NO3− content than DMPP. Even so, these inhibitors managed to reduce 64% and 96%, respectively, of the NO3−-N/NH4+-N ratio compared to the control treatment. Similar to soil mineral N, there were no differences in leaf δ15N values between the two nitrification inhibitors, yet at 30 DPF, δ15N values from sorghum BNI were more positive than those of DMPP. N2O emissions from DMPP-treated soil were low throughout the experiment. Nevertheless, while sorghum BNIs also maintained low N2O emissions, they were associated with a substantial N2O emission peak at 3 DPF that lasted until 7 DPF. Conclusions Our results indicate that while sorghum root exudates can reduce nitrification in field soil, even at the same efficiency as DMPP for a certain amount of time, they are not able to prevent the N pollution derived from N fertilization as DMPP does during the entire experiment. Graphic Abstract

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Biological nitrification inhibition in the rhizosphere: determining interactions and impact on microbially mediated processes and potential applications

Cited by 96 publications

References 468 publications

Inter-microbial competition for N and plant NO3− uptake rather than BNI determines soil net nitrification under intensively managed Brachiaria humidicola

Inter-microbial competition for N and plant NO3− uptake rather than BNI determines soil net nitrification under intensively managed Brachiaria humidicola

Root exudation of contrasting drought-stressed pearl millet genotypes conveys varying biological nitrification inhibition (BNI) activity

Biological and synthetic approaches to inhibiting nitrification in non-tilled Mediterranean soils

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