The consequences of niche and physiological differentiation of archaeal and bacterial ammonia oxidisers for nitrous oxide emissions

Linda Hink, Cecile Gubry-Rangin, Graeme W. Nicol, James I. Prosser

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Abstract

High and low rates of ammonium supply are believed to favour ammonia oxidising bacteria (AOB) and archaea (AOA), respectively. Although their contrasting affinities for ammonium are suggested to account for these differences, the influence of ammonia concentration on AOA and AOB has not been tested under environmental conditions. In addition, while both AOB and AOA contribute to nitrous oxide (N2O) emissions from soil, N2O yields (N2O-N produced per NO2- -N generated from ammonia oxidation) of AOA are lower, suggesting lower emissions when AOA dominate ammonia oxidation. This study tested the hypothesis that ammonium supplied continuously at low rates is preferentially oxidised by AOA, with lower N2O yield than expected for AOB-dominated processes. Soil microcosms were supplied with water, urea or a slow release, urea-based fertiliser and 1-octyne (inhibiting only AOB) was applied to distinguish AOA and AOB activity and associated N2O production. Low ammonium supply, from mineralisation of organic matter, or of the fertiliser, led to growth, ammonia oxidation and N2O production by AOA only, with low N2O yield. High ammonium supply, from free urea within the fertiliser or after urea addition, led to growth of both groups, but AOB-dominated ammonia oxidation was associated with two-fold greater N2O yield than that dominated by AOA. This study therefore demonstrates growth of both AOA and AOB at high ammonium concentration, confirms AOA dominance during low ammonium supply and suggests that slow release or organic fertilisers potentially mitigate N2O emissions through differences in niche specialisation and N2O production mechanisms in AOA and AOB.
Original languageEnglish
Pages (from-to)1084-1093
Number of pages10
JournalThe ISME Journal
Volume12
Early online date31 Jan 2018
DOIs
Publication statusPublished - 2018

Fingerprint

Nitrous Oxide
nitrous oxide
Ammonia
oxidants
Archaea
niche
niches
ammonia
Ammonium Compounds
Bacteria
bacterium
ammonium
bacteria
Fertilizers
urea
Urea
fertilizer
oxidation
fertilizers
Soil

Keywords

  • soil microbiology
  • nitrous oxide
  • nitrification
  • ammonia oxidisers
  • diversity
  • archaea

Cite this

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title = "The consequences of niche and physiological differentiation of archaeal and bacterial ammonia oxidisers for nitrous oxide emissions",
abstract = "High and low rates of ammonium supply are believed to favour ammonia oxidising bacteria (AOB) and archaea (AOA), respectively. Although their contrasting affinities for ammonium are suggested to account for these differences, the influence of ammonia concentration on AOA and AOB has not been tested under environmental conditions. In addition, while both AOB and AOA contribute to nitrous oxide (N2O) emissions from soil, N2O yields (N2O-N produced per NO2- -N generated from ammonia oxidation) of AOA are lower, suggesting lower emissions when AOA dominate ammonia oxidation. This study tested the hypothesis that ammonium supplied continuously at low rates is preferentially oxidised by AOA, with lower N2O yield than expected for AOB-dominated processes. Soil microcosms were supplied with water, urea or a slow release, urea-based fertiliser and 1-octyne (inhibiting only AOB) was applied to distinguish AOA and AOB activity and associated N2O production. Low ammonium supply, from mineralisation of organic matter, or of the fertiliser, led to growth, ammonia oxidation and N2O production by AOA only, with low N2O yield. High ammonium supply, from free urea within the fertiliser or after urea addition, led to growth of both groups, but AOB-dominated ammonia oxidation was associated with two-fold greater N2O yield than that dominated by AOA. This study therefore demonstrates growth of both AOA and AOB at high ammonium concentration, confirms AOA dominance during low ammonium supply and suggests that slow release or organic fertilisers potentially mitigate N2O emissions through differences in niche specialisation and N2O production mechanisms in AOA and AOB.",
keywords = "soil microbiology, nitrous oxide, nitrification, ammonia oxidisers, diversity, archaea",
author = "Linda Hink and Cecile Gubry-Rangin and Nicol, {Graeme W.} and Prosser, {James I.}",
note = "The authors are members of the Nitrous Oxide Research Alliance (NORA), a Marie Skłodowska-Curie ITN and research project under the EU's seventh framework program (FP7). GN is funded by the AXA Research Fund and CGR by a Royal Society University Research Fellowship (UF150571) and a Natural Environment Research Council (NERC) Standard Grant (NE/K016342/1). The authors would like to thank Dr Robin Walker and the SRUC Craibstone Estate (Aberdeen) for access to the agricultural plots, Dr Alex Douglas for statistical advice and Philipp Schleusner for assisting microcosm construction and sampling.",
year = "2018",
doi = "10.1038/s41396-017-0025-5",
language = "English",
volume = "12",
pages = "1084--1093",
journal = "The ISME Journal",
issn = "1751-7362",
publisher = "Nature Publishing Group",

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TY - JOUR

T1 - The consequences of niche and physiological differentiation of archaeal and bacterial ammonia oxidisers for nitrous oxide emissions

AU - Hink, Linda

AU - Gubry-Rangin, Cecile

AU - Nicol, Graeme W.

AU - Prosser, James I.

N1 - The authors are members of the Nitrous Oxide Research Alliance (NORA), a Marie Skłodowska-Curie ITN and research project under the EU's seventh framework program (FP7). GN is funded by the AXA Research Fund and CGR by a Royal Society University Research Fellowship (UF150571) and a Natural Environment Research Council (NERC) Standard Grant (NE/K016342/1). The authors would like to thank Dr Robin Walker and the SRUC Craibstone Estate (Aberdeen) for access to the agricultural plots, Dr Alex Douglas for statistical advice and Philipp Schleusner for assisting microcosm construction and sampling.

PY - 2018

Y1 - 2018

N2 - High and low rates of ammonium supply are believed to favour ammonia oxidising bacteria (AOB) and archaea (AOA), respectively. Although their contrasting affinities for ammonium are suggested to account for these differences, the influence of ammonia concentration on AOA and AOB has not been tested under environmental conditions. In addition, while both AOB and AOA contribute to nitrous oxide (N2O) emissions from soil, N2O yields (N2O-N produced per NO2- -N generated from ammonia oxidation) of AOA are lower, suggesting lower emissions when AOA dominate ammonia oxidation. This study tested the hypothesis that ammonium supplied continuously at low rates is preferentially oxidised by AOA, with lower N2O yield than expected for AOB-dominated processes. Soil microcosms were supplied with water, urea or a slow release, urea-based fertiliser and 1-octyne (inhibiting only AOB) was applied to distinguish AOA and AOB activity and associated N2O production. Low ammonium supply, from mineralisation of organic matter, or of the fertiliser, led to growth, ammonia oxidation and N2O production by AOA only, with low N2O yield. High ammonium supply, from free urea within the fertiliser or after urea addition, led to growth of both groups, but AOB-dominated ammonia oxidation was associated with two-fold greater N2O yield than that dominated by AOA. This study therefore demonstrates growth of both AOA and AOB at high ammonium concentration, confirms AOA dominance during low ammonium supply and suggests that slow release or organic fertilisers potentially mitigate N2O emissions through differences in niche specialisation and N2O production mechanisms in AOA and AOB.

AB - High and low rates of ammonium supply are believed to favour ammonia oxidising bacteria (AOB) and archaea (AOA), respectively. Although their contrasting affinities for ammonium are suggested to account for these differences, the influence of ammonia concentration on AOA and AOB has not been tested under environmental conditions. In addition, while both AOB and AOA contribute to nitrous oxide (N2O) emissions from soil, N2O yields (N2O-N produced per NO2- -N generated from ammonia oxidation) of AOA are lower, suggesting lower emissions when AOA dominate ammonia oxidation. This study tested the hypothesis that ammonium supplied continuously at low rates is preferentially oxidised by AOA, with lower N2O yield than expected for AOB-dominated processes. Soil microcosms were supplied with water, urea or a slow release, urea-based fertiliser and 1-octyne (inhibiting only AOB) was applied to distinguish AOA and AOB activity and associated N2O production. Low ammonium supply, from mineralisation of organic matter, or of the fertiliser, led to growth, ammonia oxidation and N2O production by AOA only, with low N2O yield. High ammonium supply, from free urea within the fertiliser or after urea addition, led to growth of both groups, but AOB-dominated ammonia oxidation was associated with two-fold greater N2O yield than that dominated by AOA. This study therefore demonstrates growth of both AOA and AOB at high ammonium concentration, confirms AOA dominance during low ammonium supply and suggests that slow release or organic fertilisers potentially mitigate N2O emissions through differences in niche specialisation and N2O production mechanisms in AOA and AOB.

KW - soil microbiology

KW - nitrous oxide

KW - nitrification

KW - ammonia oxidisers

KW - diversity

KW - archaea

U2 - 10.1038/s41396-017-0025-5

DO - 10.1038/s41396-017-0025-5

M3 - Article

VL - 12

SP - 1084

EP - 1093

JO - The ISME Journal

JF - The ISME Journal

SN - 1751-7362

ER -