Differential contributions of ammonia oxidizers and nitrite oxidizers to nitrification in four paddy soils

Abstract

Rice paddy fields are characterized by regular flooding and nitrogen fertilization, but the functional importance of aerobic ammonia oxidizers and nitrite oxidizers under unique agricultural management is poorly understood. In this study, we report the differential contributions of ammonia-oxidizing archaea (AOA), bacteria (AOB) and nitrite-oxidizing bacteria (NOB) to nitrification in four paddy soils from different geographic regions (Zi-Yang (ZY), Jiang-Du (JD), Lei-Zhou (LZ) and Jia-Xing (JX)) that are representative of the rice ecosystems in China. In urea-amended microcosms, nitrification activity varied greatly with 11.9, 9.46, 3.03 and 1.43 μg NO3−-N g−1 dry weight of soil per day in the ZY, JD, LZ and JX soils, respectively, over the course of a 56-day incubation period. Real-time quantitative PCR of amoA genes and pyrosequencing of 16S rRNA genes revealed significant increases in the AOA population to various extents, suggesting that their relative contributions to ammonia oxidation activity decreased from ZY to JD to LZ. The opposite trend was observed for AOB, and the JX soil stimulated only the AOB populations. DNA-based stable-isotope probing further demonstrated that active AOA numerically outcompeted their bacterial counterparts by 37.0-, 10.5- and 1.91-fold in 13C-DNA from ZY, JD and LZ soils, respectively, whereas AOB, but not AOA, were labeled in the JX soil during active nitrification. NOB were labeled to a much greater extent than AOA and AOB, and the addition of acetylene completely abolished the assimilation of 13CO2 by nitrifying populations. Phylogenetic analysis suggested that archaeal ammonia oxidation was predominantly catalyzed by soil fosmid 29i4-related AOA within the soil group 1.1b lineage. Nitrosospira cluster 3-like AOB performed most bacterial ammonia oxidation in the ZY, LZ and JX soils, whereas the majority of the 13C-AOB in the JD soil was affiliated with the Nitrosomona communis lineage. The 13C-NOB was overwhelmingly dominated by Nitrospira rather than Nitrobacter. A significant correlation was observed between the active AOA/AOB ratio and the soil oxidation capacity, implying a greater advantage of AOA over AOB under microaerophilic conditions. These results suggest the important roles of soil physiochemical properties in determining the activities of ammonia oxidizers and nitrite oxidizers.

Ammonia Oxidizing Archaea and Bacteria in East Asian Paddy Soils—A Mini Review

“…These results were further supported by a study on different Chinese paddy soils where the AOA to AOB ratio varied from 22.9 to 667 [23]. A similar trend was observed in acidic paddy soils, where the pH ranged from 4.4 to 6.8 [27,29]. These findings are corroborated by the results of Chen et al (2011) [10], who found that AOA amoA genes outnumbered AOB amoA genes in acidic paddy soils.…”

“…This technique employs a pairwise comparison of 13 CO 2 (labeled microcosms) and 12 CO 2 (control treatment) to assess whether the 13 CO 2 is assimilated by ammonia oxidizers for autotrophic growth. The result of the DNA-based stable-isotope probing technique on paddy fields across southern China showed that AOA was more active in alkaline soils whereas AOB was more active in neutral soils [29]. However, the data on paddy soils from southwestern China [34] demonstrated that nitrification was mainly attributed to AOA in acidic soils, whereas AOB was mainly responsible for nitrification in alkaline soils.…”

“…These findings are corroborated by the results of Chen et al (2011) [10], who found that AOA amoA genes outnumbered AOB amoA genes in acidic paddy soils. The results from paddy alkaline soils showed that the AOA to AOB ratio varied between 2.6 and 121.9 [11,29]. Moreover, the study on paddy soils from Hussain et al (2011) [3] showed that the relative ratio of AOA to AOB ranged from 1.46 to 3.8 and rice plant cultivation increased the AOA and AOB amoA gene abundance in the rhizosphere.…”

“…The first, lower left quadrant, is a grouping of studies that can be characterized as having alkaline and neutral soils with low ammonium concentrations. As can be seen from Figure 3, two thirds of the studies [11,[29][30][31] observed in this low ammonium concentration (below approximately 25 mg/kg) and low AOA/AOB ratios (below 100) had alkaline paddy soils. When viewing the points within the confines of this quadrant, we can characterize the activity ratio of AOA/AOB as higher in more neutral/nutrient abundant studies.…”

Long‐term fertilization regimes change soil nitrification potential by impacting active autotrophic ammonia oxidizers and nitrite oxidizers as assessed by DNA stable isotope probing

“…This ecological fitness and niche adaptation may have strongly supported the active cell division of the Nitrososphaera subcluster 1.1 in the CK and OF treatments, with soil pH values of 7.25 and 7.79 (Supporting Information Table S1) respectively. However, the lower richness of AOA in this study was likely due to our concentration solely on the active AOA and not on the overall community, an observation also made in other DNA-SIP studies (Xia et al, 2011;Wang et al, 2015a). However, the lower richness of AOA in this study was likely due to our concentration solely on the active AOA and not on the overall community, an observation also made in other DNA-SIP studies (Xia et al, 2011;Wang et al, 2015a).…”