Revisiting plant biological nitrification inhibition efficiency using multiple archaeal and bacterial ammonia-oxidising cultures

AbstractNitrification is a major process within the nitrogen (N) cycle leading to global losses of N, including fertiliser N, from natural and agricultural systems and producing significant nitrous oxide emissions. One strategy for the mitigation of these losses involves nitrification inhibition by plant-derived biological nitrification inhibitors (BNIs). Cultivation-based studies of BNIs, including screening for new compounds, have predominantly investigated inhibition of a single ammonia-oxidising bacterium (AOB), Nitrosomonas europaea, even though ammonia oxidation in soil is usually dominated by ammonia-oxidising archaea (AOA), especially in acidic soils, and AOB Nitrosospira sp., rather than Nitrosomonas, in fertilised soils. This study aimed to assess the sensitivity of ammonia oxidation by a range of AOA and AOB pure cultures to BNIs produced by plant roots (methyl 3-(4-hydroxyphenyl) propionate, sakuranetin and 1,9-decanediol) and shoots (linoleic acid, linolenic acid and methyl linoleate). AOA were generally more sensitive to BNIs than AOB, and sensitivity was greater to BNIs produced by shoots than those produced by roots. Sensitivity also varied within AOA and AOB cultures and between different BNIs. In general, N. europaea was not a good indicator of BNI inhibition, and findings therefore highlight the limitations of use of a single bioassay strain and suggest the use of a broader range of strains that are more representative of natural soil communities.

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

FEMS Microbiology Reviews ◽

10.1093/femsre/fuaa037 ◽

2020 ◽

Vol 44 (6) ◽

pp. 874-908

Author(s):

Pierfrancesco Nardi ◽

Hendrikus J Laanbroek ◽

Graeme W Nicol ◽

Giancarlo Renella ◽

Massimiliano Cardinale ◽

...

Keyword(s):

Ammonia Oxidation ◽

Natural Phenomenon ◽

Nitrification Inhibitors ◽

Nitrification Inhibition ◽

Microbial Conversion ◽

N Losses ◽

N2o Production ◽

N Transformations ◽

Potential Applications ◽

Biological Nitrification

ABSTRACT Nitrification is the microbial conversion of reduced forms of nitrogen (N) to nitrate (NO3−), and in fertilized soils it can lead to substantial N losses via NO3− leaching or nitrous oxide (N2O) production. To limit such problems, synthetic nitrification inhibitors have been applied but their performance differs between soils. In recent years, there has been an increasing interest in the occurrence of biological nitrification inhibition (BNI), a natural phenomenon according to which certain plants can inhibit nitrification through the release of active compounds in root exudates. Here, we synthesize the current state of research but also unravel knowledge gaps in the field. The nitrification process is discussed considering recent discoveries in genomics, biochemistry and ecology of nitrifiers. Secondly, we focus on the ‘where’ and ‘how’ of BNI. The N transformations and their interconnections as they occur in, and are affected by, the rhizosphere, are also discussed. The NH4+ and NO3− retention pathways alternative to BNI are reviewed as well. We also provide hypotheses on how plant compounds with putative BNI ability can reach their targets inside the cell and inhibit ammonia oxidation. Finally, we discuss a set of techniques that can be successfully applied to solve unresearched questions in BNI studies.

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A 2-yr field assessment of the effects of chemical and biological nitrification inhibitors on nitrous oxide emissions and nitrogen use efficiency in an intensively managed vegetable cropping system

Agriculture Ecosystems & Environment ◽

10.1016/j.agee.2014.12.003 ◽

2015 ◽

Vol 201 ◽

pp. 43-50 ◽

Cited By ~ 50

Author(s):

M. Zhang ◽

C.H. Fan ◽

Q.L. Li ◽

B. Li ◽

Y.Y. Zhu ◽

...

Keyword(s):

Nitrous Oxide ◽

Nitrogen Use Efficiency ◽

Cropping System ◽

Nitrous Oxide Emissions ◽

Nitrification Inhibitors ◽

Nitrogen Use ◽

Field Assessment ◽

Use Efficiency ◽

Biological Nitrification ◽

Intensively Managed

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ROOT EXUDATES FROM CANOLA EXHIBIT BIOLOGICAL NITRIFICATION INHIBITION AND ARE EFFECTIVE IN INHIBITING AMMONIA OXIDATION IN SOIL

Frontiers of Agricultural Science and Engineering ◽

10.15302/j-fase-2021421 ◽

2021 ◽

Vol 0 (0) ◽

pp. 0

Keyword(s):

Root Exudates ◽

Ammonia Oxidation ◽

Nitrification Inhibition ◽

Biological Nitrification

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Evidence of differences in nitrous oxide emissions and biological nitrification inhibition among Elymus grass species

Biology and Fertility of Soils ◽

10.1007/s00374-021-01592-y ◽

2021 ◽

Author(s):

Wang Li ◽

Jianguo Ma ◽

Saman Bowatte ◽

Coby Hoogendoorn ◽

Fujiang Hou

Keyword(s):

Nitrous Oxide ◽

Nitrous Oxide Emissions ◽

Grass Species ◽

Nitrification Inhibition ◽

Biological Nitrification

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Biological nitrification inhibition by Brachiaria grasses mitigates soil nitrous oxide emissions from bovine urine patches

Soil Biology and Biochemistry ◽

10.1016/j.soilbio.2016.12.029 ◽

2017 ◽

Vol 107 ◽

pp. 156-163 ◽

Cited By ~ 43

Author(s):

Ryan C. Byrnes ◽

Jonathan Nùñez ◽

Laura Arenas ◽

Idupulapati Rao ◽

Catalina Trujillo ◽

...

Keyword(s):

Nitrous Oxide ◽

Nitrous Oxide Emissions ◽

Nitrification Inhibition ◽

Bovine Urine ◽

Biological Nitrification

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4-Amino-1,2,4-triazole can be more effective than commercial nitrification inhibitors at high soil temperatures

Soil Research ◽

10.1071/sr16340 ◽

2017 ◽

Vol 55 (7) ◽

pp. 715 ◽

Cited By ~ 2

Author(s):

Tariq Mahmood ◽

Rehmat Ali ◽

Asma Lodhi ◽

Muhammad Sajid

Keyword(s):

Inhibitory Effect ◽

Application Rate ◽

Climatic Conditions ◽

Nitrification Inhibitors ◽

Nitrification Inhibition ◽

N Accumulation ◽

Different Temperatures ◽

Soil Temperatures ◽

Summer Temperatures ◽

New Compounds

Commercial nitrification inhibitors (NIs), namely nitrapyrin, 3,4-dimethylpyrazol phosphate (DMPP) and dicyandiamide (DCD), are ineffective at high temperatures. Therefore, it is imperative to explore new compounds that can be commercialised as effective NIs for warm climatic conditions. The aim of the present study was to compare the potential of 4-amino-1,2,4-triazole (ATC) with the two commercial NIs DMPP and DCD to delay nitrification of (NH4)2SO4 in an alkaline calcareous soil incubated under aerobic conditions at warm temperatures (35 and 25°C). Inhibitors were incorporated in (NH4)2SO4 granules and nitrification inhibition was calculated on the basis of net NH4+-N disappearance and net NO3–-N accumulation. At 35°C, the inhibitory effect of DCD and DMPP persisted only for 1 week, whereas ATC was effective up to 4 weeks. At 25°C, the inhibitory effect of ATC, DMPP and DCD was comparable. In another set of experiments, different concentrations of ATC (0.25–6% of N) were tested at three different temperatures (35, 25 and 18°C). At 35°C, ATC applied at 2% of N caused 63% inhibition for 2 weeks, whereas at a rate of 4–6% of N the inhibitory effect of ATC persisted up to 4 weeks (63–84% inhibition). At 25°C, ATC application at a rate of 1% of N caused 64% inhibition for 2 weeks; increasing the application rate to 2–6% of N prolonged the inhibitory effect up to 4 weeks (55–94% inhibition). At 18°C, a much lower concentration of ATC (0.25–0.5% of N) was required to achieve ≥50% inhibition for 2–4 weeks, whereas increasing the application rate to 2% of N caused 93% inhibition for 4 weeks. The results of the present study suggest that although commercially available NIs are ineffective at high summer temperatures, ATC may have the potential to be commercialised as an effective NI for warm as well as moderate climatic conditions.

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Marine ammonia-oxidising archaea and bacteria occupy distinct iron and copper niches

ISME Communications ◽

10.1038/s43705-021-00001-7 ◽

2021 ◽

Vol 1 (1) ◽

Author(s):

Roxana T. Shafiee ◽

Poppy J. Diver ◽

Joseph T. Snow ◽

Qiong Zhang ◽

Rosalind E. M. Rickaby

Keyword(s):

Comparative Genomics ◽

Trace Metals ◽

Trace Metal ◽

Ammonia Oxidation ◽

Testable Hypothesis ◽

Niche Separation ◽

Toxicity Threshold ◽

Geologic Time ◽

Additional Explanation ◽

Ammonia Oxidising Archaea

AbstractAmmonia oxidation by archaea and bacteria (AOA and AOB), is the first step of nitrification in the oceans. As AOA have an ammonium affinity 200-fold higher than AOB isolates, the chemical niche allowing AOB to persist in the oligotrophic ocean remains unclear. Here we show that marine isolates, Nitrosopumilus maritimus strain SCM1 (AOA) and Nitrosococcus oceani strain C-107 (AOB) have contrasting physiologies in response to the trace metals iron (Fe) and copper (Cu), holding potential implications for their niche separation in the oceans. A greater affinity for unchelated Fe may allow AOB to inhabit shallower, euphotic waters where ammonium supply is high, but competition for Fe is rife. In contrast to AOB, AOA isolates have a greater affinity and toxicity threshold for unchelated Cu providing additional explanation to the greater success of AOA in the marine environment where Cu availability can be highly variable. Using comparative genomics, we predict that the proteomic and metal transport basis giving rise to contrasting physiologies in isolates is widespread across phylogenetically diverse marine AOA and AOB that are not yet available in pure culture. Our results develop the testable hypothesis that ammonia oxidation may be limited by Cu in large tracts of the open ocean and suggest a relatively earlier emergence of AOB than AOA when considered in the context of evolving trace metal availabilities over geologic time.

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Biological nitrification inhibition in maize—isolation and identification of hydrophobic inhibitors from root exudates

Biology and Fertility of Soils ◽

10.1007/s00374-021-01577-x ◽

2021 ◽

Author(s):

Junnosuke Otaka ◽

Guntur Venkata Subbarao ◽

Hiroshi Ono ◽

Tadashi Yoshihashi

Keyword(s):

Root Exudation ◽

Root Systems ◽

Root Surface ◽

Maize Root ◽

Nitrification Inhibition ◽

Isolation And Identification ◽

N Losses ◽

Chemical Structures ◽

Maize Roots ◽

Biological Nitrification

AbstractTo control agronomic N losses and reduce environmental pollution, biological nitrification inhibition (BNI) is a promising strategy. BNI is an ecological phenomenon by which certain plants release bioactive compounds that can suppress nitrifying soil microbes. Herein, we report on two hydrophobic BNI compounds released from maize root exudation (1 and 2), together with two BNI compounds inside maize roots (3 and 4). On the basis of a bioassay-guided fractionation method using a recombinant nitrifying bacterium Nitrosomonas europaea, 2,7-dimethoxy-1,4-naphthoquinone (1, ED50 = 2 μM) was identified for the first time from dichloromethane (DCM) wash concentrate of maize root surface and named “zeanone.” The benzoxazinoid 2-hydroxy-4,7-dimethoxy-2H-1,4-benzoxazin-3(4H)-one (HDMBOA, 2, ED50 = 13 μM) was isolated from DCM extract of maize roots, and two analogs of compound 2, 2-hydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one (HMBOA, 3, ED50 = 91 μM) and HDMBOA-β-glucoside (4, ED50 = 94 μM), were isolated from methanol extract of maize roots. Their chemical structures (1–4) were determined by extensive spectroscopic methods. The contributions of these four isolated BNI compounds (1–4) to the hydrophobic BNI activity in maize roots were 19%, 20%, 2%, and 4%, respectively. A possible biosynthetic pathway for zeanone (1) is proposed. These results provide insights into the strength of hydrophobic BNI activity released from maize root systems, the chemical identities of the isolated BNIs, and their relative contribution to the BNI activity from maize root systems.

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