Nitrous oxide production by ammonia oxidisers: Physiological diversity, niche differentiation and potential mitigation strategies

James I Prosser* (Corresponding Author), Linda Hink, Cécile Gubry-Rangin, Graeme W. Nicol

*Corresponding author for this work

Research output: Contribution to journalReview article

1 Citation (Scopus)

Abstract

Oxidation of ammonia to nitrite by bacteria and archaea is responsible for global emissions of nitrous oxide directly and indirectly through provision of nitrite and, after further oxidation, nitrate to denitrifiers. Their contributions to increasing N2 O emissions are greatest in terrestrial environments, due to the dramatic and continuing increases in use of ammonia-based fertilisers, which have been driven by requirement for increased food production, but which also provide a source of energy for ammonia oxidisers, leading to an imbalance in the terrestrial nitrogen cycle. Direct N2 O production by ammonia oxidisers results from several metabolic processes, sometimes combined with abiotic reactions. Physiological characteristics, including mechanisms for N2 O production, vary within and between ammonia oxidising archaea (AOA) and bacteria (AOB) and comammox bacteria and N2 O yield of AOB is higher than in the last two groups. There is also strong evidence for niche differentiation between AOA and AOB with respect to environmental conditions in natural and engineered environments. In particular, AOA are favoured by low soil pH and AOA and AOB are respectively favoured by low rates of ammonium supply, equivalent to application of slow-release fertiliser, or high rates of supply, equivalent to addition of high concentrations of inorganic ammonium or urea. These differences between AOA and AOB provide the potential for better fertilisation strategies that could both increase fertiliser use efficiency and reduce N2 O emissions from agricultural soils. This article reviews research on the biochemistry, physiology and ecology of ammonia oxidisers and discusses the consequences for ammonia oxidiser communities subjected to different agricultural practices and the ways in which this knowledge, coupled with improved methods for characterising communities, might lead to improved fertiliser use efficiency and mitigation of N2 O emissions.

Original languageEnglish
Pages (from-to)103-118
Number of pages16
JournalGlobal Change Biology
Volume26
Issue number1
Early online date29 Nov 2019
DOIs
Publication statusPublished - Jan 2020

Fingerprint

Nitrous Oxide
nitrous oxide
Ammonia
niche
mitigation
ammonia
Bacteria
Fertilizers
bacterium
fertilizer
Nitrites
Ammonium Compounds
nitrite
ammonium
Soils
oxidation
Oxidation
Biochemistry
nitrogen cycle
biochemistry

Keywords

  • archaeal ammonia oxidisers
  • bacterial ammonia oxidisers
  • nitrification, nitrous oxide emissions
  • soil
  • marine
  • agriculture

Cite this

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title = "Nitrous oxide production by ammonia oxidisers: Physiological diversity, niche differentiation and potential mitigation strategies",
abstract = "Oxidation of ammonia to nitrite by bacteria and archaea is responsible for global emissions of nitrous oxide directly and indirectly through provision of nitrite and, after further oxidation, nitrate to denitrifiers. Their contributions to increasing N2 O emissions are greatest in terrestrial environments, due to the dramatic and continuing increases in use of ammonia-based fertilisers, which have been driven by requirement for increased food production, but which also provide a source of energy for ammonia oxidisers, leading to an imbalance in the terrestrial nitrogen cycle. Direct N2 O production by ammonia oxidisers results from several metabolic processes, sometimes combined with abiotic reactions. Physiological characteristics, including mechanisms for N2 O production, vary within and between ammonia oxidising archaea (AOA) and bacteria (AOB) and comammox bacteria and N2 O yield of AOB is higher than in the last two groups. There is also strong evidence for niche differentiation between AOA and AOB with respect to environmental conditions in natural and engineered environments. In particular, AOA are favoured by low soil pH and AOA and AOB are respectively favoured by low rates of ammonium supply, equivalent to application of slow-release fertiliser, or high rates of supply, equivalent to addition of high concentrations of inorganic ammonium or urea. These differences between AOA and AOB provide the potential for better fertilisation strategies that could both increase fertiliser use efficiency and reduce N2 O emissions from agricultural soils. This article reviews research on the biochemistry, physiology and ecology of ammonia oxidisers and discusses the consequences for ammonia oxidiser communities subjected to different agricultural practices and the ways in which this knowledge, coupled with improved methods for characterising communities, might lead to improved fertiliser use efficiency and mitigation of N2 O emissions.",
keywords = "archaeal ammonia oxidisers, bacterial ammonia oxidisers, nitrification, nitrous oxide emissions, soil, marine, agriculture",
author = "Prosser, {James I} and Linda Hink and C{\'e}cile Gubry-Rangin and Nicol, {Graeme W.}",
note = "Funding Information AXA Research Fund Royal Society. Grant Number: UF150571 FP7 People: Marie‐Curie Actions ITN",
year = "2020",
month = "1",
doi = "10.1111/gcb.14877",
language = "English",
volume = "26",
pages = "103--118",
journal = "Global Change Biology",
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publisher = "John Wiley & Sons, Ltd (10.1111)",
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TY - JOUR

T1 - Nitrous oxide production by ammonia oxidisers

T2 - Physiological diversity, niche differentiation and potential mitigation strategies

AU - Prosser, James I

AU - Hink, Linda

AU - Gubry-Rangin, Cécile

AU - Nicol, Graeme W.

N1 - Funding Information AXA Research Fund Royal Society. Grant Number: UF150571 FP7 People: Marie‐Curie Actions ITN

PY - 2020/1

Y1 - 2020/1

N2 - Oxidation of ammonia to nitrite by bacteria and archaea is responsible for global emissions of nitrous oxide directly and indirectly through provision of nitrite and, after further oxidation, nitrate to denitrifiers. Their contributions to increasing N2 O emissions are greatest in terrestrial environments, due to the dramatic and continuing increases in use of ammonia-based fertilisers, which have been driven by requirement for increased food production, but which also provide a source of energy for ammonia oxidisers, leading to an imbalance in the terrestrial nitrogen cycle. Direct N2 O production by ammonia oxidisers results from several metabolic processes, sometimes combined with abiotic reactions. Physiological characteristics, including mechanisms for N2 O production, vary within and between ammonia oxidising archaea (AOA) and bacteria (AOB) and comammox bacteria and N2 O yield of AOB is higher than in the last two groups. There is also strong evidence for niche differentiation between AOA and AOB with respect to environmental conditions in natural and engineered environments. In particular, AOA are favoured by low soil pH and AOA and AOB are respectively favoured by low rates of ammonium supply, equivalent to application of slow-release fertiliser, or high rates of supply, equivalent to addition of high concentrations of inorganic ammonium or urea. These differences between AOA and AOB provide the potential for better fertilisation strategies that could both increase fertiliser use efficiency and reduce N2 O emissions from agricultural soils. This article reviews research on the biochemistry, physiology and ecology of ammonia oxidisers and discusses the consequences for ammonia oxidiser communities subjected to different agricultural practices and the ways in which this knowledge, coupled with improved methods for characterising communities, might lead to improved fertiliser use efficiency and mitigation of N2 O emissions.

AB - Oxidation of ammonia to nitrite by bacteria and archaea is responsible for global emissions of nitrous oxide directly and indirectly through provision of nitrite and, after further oxidation, nitrate to denitrifiers. Their contributions to increasing N2 O emissions are greatest in terrestrial environments, due to the dramatic and continuing increases in use of ammonia-based fertilisers, which have been driven by requirement for increased food production, but which also provide a source of energy for ammonia oxidisers, leading to an imbalance in the terrestrial nitrogen cycle. Direct N2 O production by ammonia oxidisers results from several metabolic processes, sometimes combined with abiotic reactions. Physiological characteristics, including mechanisms for N2 O production, vary within and between ammonia oxidising archaea (AOA) and bacteria (AOB) and comammox bacteria and N2 O yield of AOB is higher than in the last two groups. There is also strong evidence for niche differentiation between AOA and AOB with respect to environmental conditions in natural and engineered environments. In particular, AOA are favoured by low soil pH and AOA and AOB are respectively favoured by low rates of ammonium supply, equivalent to application of slow-release fertiliser, or high rates of supply, equivalent to addition of high concentrations of inorganic ammonium or urea. These differences between AOA and AOB provide the potential for better fertilisation strategies that could both increase fertiliser use efficiency and reduce N2 O emissions from agricultural soils. This article reviews research on the biochemistry, physiology and ecology of ammonia oxidisers and discusses the consequences for ammonia oxidiser communities subjected to different agricultural practices and the ways in which this knowledge, coupled with improved methods for characterising communities, might lead to improved fertiliser use efficiency and mitigation of N2 O emissions.

KW - archaeal ammonia oxidisers

KW - bacterial ammonia oxidisers

KW - nitrification, nitrous oxide emissions

KW - soil

KW - marine

KW - agriculture

U2 - 10.1111/gcb.14877

DO - 10.1111/gcb.14877

M3 - Review article

C2 - 31638306

VL - 26

SP - 103

EP - 118

JO - Global Change Biology

JF - Global Change Biology

SN - 1354-1013

IS - 1

ER -