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The diversity of the N2O reducers matters for the N2O:N2 denitrification end-product ratio across an annual and a perennial cropping system.

Domeignoz-Horta LA, Spor A, Bru D, Breuil MC, Bizouard F, Léonard J, Philippot L - Front Microbiol (2015)

Bottom Line: The abundance of N2O-reducers and producers was quantified by real-time PCR, and the diversity of both nosZ clades was determined by 454 pyrosequencing.Overall, the results showed limited differences between management practices but there were significant differences between cropping systems in both the abundance and structure of the nosZII community, as well as in the [rN2O/r(N2O+N2)] ratio.Potential denitrification activity and potential N2O production were explained mainly by the soil properties while the diversity of the nosZII clade on its own explained 26% of the denitrification end-product ratio, which highlights the importance of understanding the ecology of this newly identified clade of N2O reducers for mitigation strategies.

View Article: PubMed Central - PubMed

Affiliation: INRA, UMR 1347 Agroécologie Dijon, France.

ABSTRACT
Agriculture is the main source of terrestrial emissions of N2O, a potent greenhouse gas and the main cause of ozone layer depletion. The reduction of N2O into N2 by microorganisms carrying the nitrous oxide reductase gene (nosZ) is the only biological process known to eliminate this greenhouse gas. Recent studies showed that a previously unknown clade of N2O-reducers was related to the capacity of the soil to act as an N2O sink, opening the way for new strategies to mitigate emissions. Here, we investigated whether the agricultural practices could differently influence the two N2O reducer clades with consequences for denitrification end-products. The abundance of N2O-reducers and producers was quantified by real-time PCR, and the diversity of both nosZ clades was determined by 454 pyrosequencing. Potential N2O production and potential denitrification activity were used to calculate the denitrification gaseous end-product ratio. Overall, the results showed limited differences between management practices but there were significant differences between cropping systems in both the abundance and structure of the nosZII community, as well as in the [rN2O/r(N2O+N2)] ratio. More limited differences were observed in the nosZI community, suggesting that the newly identified nosZII clade is more sensitive than nosZI to environmental changes. Potential denitrification activity and potential N2O production were explained mainly by the soil properties while the diversity of the nosZII clade on its own explained 26% of the denitrification end-product ratio, which highlights the importance of understanding the ecology of this newly identified clade of N2O reducers for mitigation strategies.

No MeSH data available.


NMDS ordinations of nosZ weighted unifrac distance matrices. (A) Variation in nosZI community structure. (B) Variation in nosZII community structure. Red curves represent the final denitrification product [rN2O/r(N2O/N2)]. Significant explanatory variables are represented as blue vectors (P < 0.05), Ca (calcium g kg−1 dw soil), q.nosZII and q.nirK correspond to the quantification by qPCR of nitrous oxide reductase community (clade II) and copper nitrite reductase community, respectively (copy number g−1 dw soil); sand and water content are expressed in percentage. The lengths of the arrows are proportional to the strength of the correlation. Stress values are indicated at the bottom right of each panel.
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Figure 2: NMDS ordinations of nosZ weighted unifrac distance matrices. (A) Variation in nosZI community structure. (B) Variation in nosZII community structure. Red curves represent the final denitrification product [rN2O/r(N2O/N2)]. Significant explanatory variables are represented as blue vectors (P < 0.05), Ca (calcium g kg−1 dw soil), q.nosZII and q.nirK correspond to the quantification by qPCR of nitrous oxide reductase community (clade II) and copper nitrite reductase community, respectively (copy number g−1 dw soil); sand and water content are expressed in percentage. The lengths of the arrows are proportional to the strength of the correlation. Stress values are indicated at the bottom right of each panel.

Mentions: To assess whether the agricultural practices could drive the composition and structure of the N2O-reducer community, the diversity of both nosZI and nosZII clades was characterized by 454 pyrosequencing. 123,130 nosZI and 121,500 nosZII sequences were obtained from samples after quality filtering. Similarity-based clustering of sequences gave an average of 162 (CI95% = 133–191) and 312 (CI95% = 279–345) OTUs for nosZI and nosZII respectively in BE, and 158 (CI95% = 136–180) and 355 (CI95% = 330–380) OTUs for nosZI and nosZII respectively in ORE. In both BE and ORE, the nosZII community had a significantly higher richness than nosZI (P < 0.0001). Within BE and ORE, the agricultural practices had no significant effect on the α-diversity of the N2O-reducing communities (Table S1). An analysis of nosZI and nosZII phylogenies showed that the most abundant sequences in ORE and BE were similar (Figures S2, S3), with nosZII sequences affiliated mainly to nosZ from Bacteroidetes while nosZI sequences were affiliated to nosZ from Alphaproteobacteria and Betaproteobacteria. Further examination of the β-diversity by non-metric multidimensional scaling (NMDS) and analysis of similarity (ANOSIM) showed (Figures 2A,B) no clustering of samples according to the agricultural practices. However, differences in both nosZ communities between annual rotation and perennial cropping systems were significant, but stronger for nosZII communities, (R = 0.43, P < 0.0001 and R = 0.77, P < 0.0001 for nosZI and nosZII respectively). Fitting the environmental variables onto the ordination plot showed that pH and calcium were significant explanatory variables (P<0.05) for the community structure of both guilds. The nosZI community structure was also related to the water content while the abundance of nitrite reductase genes (nirK) and sand content were related to the nosZII community structure (Figure 2B). The [rN2O/r(N2O+N2)] surface was fitted onto the ordination plot and showed a strong relationship between the nosZII community structure, its diversity and the denitrification end products with a lower proportion of N2O produced when the nosZII diversity increased (Figure 2B).


The diversity of the N2O reducers matters for the N2O:N2 denitrification end-product ratio across an annual and a perennial cropping system.

Domeignoz-Horta LA, Spor A, Bru D, Breuil MC, Bizouard F, Léonard J, Philippot L - Front Microbiol (2015)

NMDS ordinations of nosZ weighted unifrac distance matrices. (A) Variation in nosZI community structure. (B) Variation in nosZII community structure. Red curves represent the final denitrification product [rN2O/r(N2O/N2)]. Significant explanatory variables are represented as blue vectors (P < 0.05), Ca (calcium g kg−1 dw soil), q.nosZII and q.nirK correspond to the quantification by qPCR of nitrous oxide reductase community (clade II) and copper nitrite reductase community, respectively (copy number g−1 dw soil); sand and water content are expressed in percentage. The lengths of the arrows are proportional to the strength of the correlation. Stress values are indicated at the bottom right of each panel.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4585238&req=5

Figure 2: NMDS ordinations of nosZ weighted unifrac distance matrices. (A) Variation in nosZI community structure. (B) Variation in nosZII community structure. Red curves represent the final denitrification product [rN2O/r(N2O/N2)]. Significant explanatory variables are represented as blue vectors (P < 0.05), Ca (calcium g kg−1 dw soil), q.nosZII and q.nirK correspond to the quantification by qPCR of nitrous oxide reductase community (clade II) and copper nitrite reductase community, respectively (copy number g−1 dw soil); sand and water content are expressed in percentage. The lengths of the arrows are proportional to the strength of the correlation. Stress values are indicated at the bottom right of each panel.
Mentions: To assess whether the agricultural practices could drive the composition and structure of the N2O-reducer community, the diversity of both nosZI and nosZII clades was characterized by 454 pyrosequencing. 123,130 nosZI and 121,500 nosZII sequences were obtained from samples after quality filtering. Similarity-based clustering of sequences gave an average of 162 (CI95% = 133–191) and 312 (CI95% = 279–345) OTUs for nosZI and nosZII respectively in BE, and 158 (CI95% = 136–180) and 355 (CI95% = 330–380) OTUs for nosZI and nosZII respectively in ORE. In both BE and ORE, the nosZII community had a significantly higher richness than nosZI (P < 0.0001). Within BE and ORE, the agricultural practices had no significant effect on the α-diversity of the N2O-reducing communities (Table S1). An analysis of nosZI and nosZII phylogenies showed that the most abundant sequences in ORE and BE were similar (Figures S2, S3), with nosZII sequences affiliated mainly to nosZ from Bacteroidetes while nosZI sequences were affiliated to nosZ from Alphaproteobacteria and Betaproteobacteria. Further examination of the β-diversity by non-metric multidimensional scaling (NMDS) and analysis of similarity (ANOSIM) showed (Figures 2A,B) no clustering of samples according to the agricultural practices. However, differences in both nosZ communities between annual rotation and perennial cropping systems were significant, but stronger for nosZII communities, (R = 0.43, P < 0.0001 and R = 0.77, P < 0.0001 for nosZI and nosZII respectively). Fitting the environmental variables onto the ordination plot showed that pH and calcium were significant explanatory variables (P<0.05) for the community structure of both guilds. The nosZI community structure was also related to the water content while the abundance of nitrite reductase genes (nirK) and sand content were related to the nosZII community structure (Figure 2B). The [rN2O/r(N2O+N2)] surface was fitted onto the ordination plot and showed a strong relationship between the nosZII community structure, its diversity and the denitrification end products with a lower proportion of N2O produced when the nosZII diversity increased (Figure 2B).

Bottom Line: The abundance of N2O-reducers and producers was quantified by real-time PCR, and the diversity of both nosZ clades was determined by 454 pyrosequencing.Overall, the results showed limited differences between management practices but there were significant differences between cropping systems in both the abundance and structure of the nosZII community, as well as in the [rN2O/r(N2O+N2)] ratio.Potential denitrification activity and potential N2O production were explained mainly by the soil properties while the diversity of the nosZII clade on its own explained 26% of the denitrification end-product ratio, which highlights the importance of understanding the ecology of this newly identified clade of N2O reducers for mitigation strategies.

View Article: PubMed Central - PubMed

Affiliation: INRA, UMR 1347 Agroécologie Dijon, France.

ABSTRACT
Agriculture is the main source of terrestrial emissions of N2O, a potent greenhouse gas and the main cause of ozone layer depletion. The reduction of N2O into N2 by microorganisms carrying the nitrous oxide reductase gene (nosZ) is the only biological process known to eliminate this greenhouse gas. Recent studies showed that a previously unknown clade of N2O-reducers was related to the capacity of the soil to act as an N2O sink, opening the way for new strategies to mitigate emissions. Here, we investigated whether the agricultural practices could differently influence the two N2O reducer clades with consequences for denitrification end-products. The abundance of N2O-reducers and producers was quantified by real-time PCR, and the diversity of both nosZ clades was determined by 454 pyrosequencing. Potential N2O production and potential denitrification activity were used to calculate the denitrification gaseous end-product ratio. Overall, the results showed limited differences between management practices but there were significant differences between cropping systems in both the abundance and structure of the nosZII community, as well as in the [rN2O/r(N2O+N2)] ratio. More limited differences were observed in the nosZI community, suggesting that the newly identified nosZII clade is more sensitive than nosZI to environmental changes. Potential denitrification activity and potential N2O production were explained mainly by the soil properties while the diversity of the nosZII clade on its own explained 26% of the denitrification end-product ratio, which highlights the importance of understanding the ecology of this newly identified clade of N2O reducers for mitigation strategies.

No MeSH data available.