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Mitigating N2O emissions - an ES delivered by soil microbes
Sara Hallin
Dept. Forest Mycology & Plant PathologySwedish University of Agricultural Sciences, Uppsala
ClimBEco Annual MeetingAug 24-25, 2017
Höllviken
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« the microbial zoo »
Biomass in soil: 10 ton/ha• Bacteria 1-2 ton
Bacteria occupy <0.3% of pore space
Fungi: 10 – 100 m/gBacterial cells: 107 – 1010/g
”Species”: 103 – 104/g
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N
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“Leaky pipe” – N losses from soil
N2ON2O
Leaching
NH4+ NH2OH
NitrificationNO3
- NO2- NO N2O
N2
DenitrificationNO2
-
N2O
(Philippot & Hallin 2011, Trends Plant Sci.)
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N2O
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(Redrawn from Hallin et al. 2017 Trends Microbiol.)
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NirS
NosZNORNirK
NO3- NO2
- NO N2O N2
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N
OO
O
N
OO
O
N
OO
O
N
OO
O
N
OO
O
N
OO
O
NONON2
NON2ONONONO3- NO2- Denitrification
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N
OO
O
N
OO
O
N
OO
O
N
OO
O
N
OO
O
N
OO
O
N N
N NN N
NONON2
NON2ONONONO3- NO2- Denitrification
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ON N
ON NON N
NONON2
NON2ONONONO3- NO2- Denitrification
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ON NON N
N N
N N
NONON2
NON2ONONONO3- NO2- Denitrification
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nirKnirSnornosZ
652 genomes with denitrification genes:
SSU tree
(Graf et al, 2014 PLOS ONE)
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• 30% have nosZwithout nir genes
• 24% have only nosZ –true N2O sinks
nirK+nosZ
70% of nosZ genomes have a complete denitrification pathway
(Graf et al, 2014 PLOS ONE)
Nearly 46% of 652 genomes potential N2O reducers
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(Jones et al. 2013 ISME J)
Clade I
Clade II
Denitrification pathway
(Graf et al, 2014 PLOS ONE)
A new clade of the N2O reductase - N2O sink?
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nosZ Clade I and II abundance in soils and other systems
Soil
WWTPWetland
Rice paddies Sediments
% o
f tot
al b
acte
rial c
omm
unity
(Jones et al. 2013 ISME J)
Clade IClade II
Clade I Clade II
(Orellana et al. 2014 mBio)
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Reduction of N2O produced by inherent soil microbes by inocculating Dyadobacter fermentans into arable soils:
(Domeignoz-Horta et al, 2016 Soil Biol Biochem)
• nosZ II• not capable of denitrification• not capable of N2O production• N2O reduction coupled to growth
N2O
N2O reducing strain
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No strain addedLOW inocculation levelHIGH inocculation level
First evidence that non-denitrifying N2O-reducers contribute to soil N2O reduction
Deni
trifi
catio
nen
d-pr
oduc
trat
io(N
2O/[
N2O
+ N
2])
Agricultural soils
(Domeignoz-Horta et al, 2016 Soil Biol Biochem)
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In the soil
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rN2O/r[N2+ N2O]Non-inoculated
rN2O/r[N2+ N2O]108 cells g-1 soil DW
rN2O/r[N2+ N2O]109 cells g -1 soil DW
Source
Sink
N2O s i n k i n d e
0.00.2
0.40.6
0.81.0
0.0
0.2
0.40.6
0.81.0
0.0
0.2
0.4
0.6
0.8
1.0
-0.15
-0.10
-0.05
0.00
0.05
0.10
0.15
0.20
Capacity to consume N2O:
(Jones et al, 2014 Nature Climate Change)
Range of potential soil N2O sink capacity across 47 soils
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Factors underlying N2O source or sink
Variable importanceStructural equation modeling
Factors underlying soil N2O source or sink
(Jones et al, 2014 Nature Climate Change)
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Associated with plants
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Treatments:• Sunflower• Barley• Control
• Soil A• Soil B
nosZ I
Soil A
nosZ II
Soil B
(Graf et al, manuscript)
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(Graf et al, 2016 Soil Biol Biochem)
Soil A Soil B
nosZ
II:no
sZI r
atio
Niche differentiation between clade I and clade II
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(Graf et al, manuscript)
Net
Rel
ated
ness
Inde
x (N
RI)
nosZ I nosZ I
nosZ II nosZ II
Soil A Soil B
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Farming system & practices
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14 long-term trials, +/-N
(Putz et al, manuscript)
Deni
trifi
catio
n en
d pr
oduc
t rat
io(N
2O/(
N2O
+N2)
)
nosZ/nir gene abundance
r2 = 0.49p < 0.0001
Long-term effects of N-fertilization on N2O reducers
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***
Rela
tive
Abun
canc
e [%
]
*** **
Effect of site on the nosZ clade I community structure
Effect of site and fertilization on the nosZ clade II community structure**
* * **
% c
hang
efr
om u
nfer
tlize
d
nirS
nosZ InirK
NO3- NO2
- NO N2O N2
nosZ II
(Putz et al, manuscript)
Specific taxa change and abundance of denitrifiers increase
Community structure of N2O reducers:
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N kg ha-1 y-1 0 150 0 120Soil C:NO3
- 0.64 0.70 0.55 0.50
NO3- NO2
- nir nosZNO2-NH4
+ nrfA NO N2O N2
(Schleusner et al, manuscript)
Long-term effects of cropping system on fate of nitrate
Denitrification
Dissimilatorty nitrate reduction to ammonium
(DNRA)
Nitrogen lossNitrogen retention
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Cropping system overrule fertilization
C to nitrate ratio drives differences
Ley more DNRA activity and less N2O emissions, confirms gene data
DNRA bacteria : DenitrifiersN2O reducers : Denitrifiers
(Schleusner et al, manuscript)
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Ecosystem scale
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(Juhanson et al, 2017 SBB; Enwall et al, 2010 AEM)
• α diversity, abundance, comunity structure, assemblymechansims show nichedifferentiation
• Suggest biotic interactions drive nosZ clade II microbes
Spatial study of clade I and II nosZ communities across 44 ha
nirK abundancenosZI/nosZII
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ON NON N
N N
N N
NONON2
NON2ONONONO3- NO2- Denitrification
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Agricultural Diversification – Digging Deeper
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Oscar and Lili LammFoundation
INRA, France:Laurent PhilippotDavid BruLuiz Domeignoz-HortaAymé Spor
Univ. Gothenburg:Philipp SchleusnerTobias Rütting
Microbial Ecology:Chris JonesDaniel GrafMartina PutzMaren EmmerichMing ZhaoMaria HellmanJaanis Juhansson
Awesome team Collaborators Funding
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PhD position on fungal denitrification openingContact me: [email protected]
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HI: Agricultural Diversification enhances Soil Biodiversity and EcosystemSustainability
(Bender et al. 2017. Trends Ecol Evol)