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Phylogenetically distinct phylotypes modulate nitrification in a paddy soil.

ABSTRACT: Paddy fields represent a unique ecosystem in which regular flooding occurs, allowing for rice cultivation. However, the taxonomic identity of the microbial functional guilds that catalyze soil nitrification remains poorly understood. In this study, we provide molecular evidence for distinctly different phylotypes of nitrifying communities in a neutral paddy soil using high-throughput pyrosequencing and DNA-based stable isotope probing (SIP). Following urea addition, the levels of soil nitrate increased significantly, accompanied by an increase in the abundance of the bacterial and archaeal amoA gene in microcosms subjected to SIP (SIP microcosms) during a 56-day incubation period. High-throughput fingerprints of the total 16S rRNA genes in SIP microcosms indicated that nitrification activity positively correlated with the abundance of Nitrosospira-like ammonia-oxidizing bacteria (AOB), soil group 1.1b-like ammonia-oxidizing archaea (AOA), and Nitrospira-like nitrite-oxidizing bacteria (NOB). Pyrosequencing of 13C-labeled DNA further revealed that 13CO2 was assimilated by these functional groups to a much greater extent than by marine group 1.1a-associated AOA and Nitrobacter-like NOB. Phylogenetic analysis demonstrated that active AOB communities were closely affiliated with Nitrosospira sp. strain L115 and the Nitrosospira multiformis lineage and that the 13C-labeled AOA were related to phylogenetically distinct groups, including the moderately thermophilic "Candidatus Nitrososphaera gargensis," uncultured fosmid 29i4, and acidophilic "Candidatus Nitrosotalea devanaterra" lineages. These results suggest that a wide variety of microorganisms were involved in soil nitrification, implying physiological diversification of soil nitrifying communities that are constantly exposed to environmental fluctuations in paddy fields.

SUBMITTER: Zhao J

PROVIDER: S-EPMC4393434 | biostudies-literature | 2015 May

REPOSITORIES: biostudies-literature

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Phylogenetically distinct phylotypes modulate nitrification in a paddy soil.

Zhao Jun J Wang Baozhan B Jia Zhongjun Z

Applied and environmental microbiology 20150227 9

Paddy fields represent a unique ecosystem in which regular flooding occurs, allowing for rice cultivation. However, the taxonomic identity of the microbial functional guilds that catalyze soil nitrification remains poorly understood. In this study, we provide molecular evidence for distinctly different phylotypes of nitrifying communities in a neutral paddy soil using high-throughput pyrosequencing and DNA-based stable isotope probing (SIP). Following urea addition, the levels of soil nitrate in ...[more]

PMID: 25724959

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Project description:IntroductionSoil ammonia oxidation, which acts as the first and rate-limiting step of nitrification, is driven by ammonia-oxidizing bacteria (AOB), ammonia-oxidizing archaea (AOA) and complete ammonia oxidizer (comammox, amoA gene of clade-A and clade-B). Straw returning, widely used ecological technology in China, is an effective measure for promoting straw decomposition and soil nutrient cycling when combined with earthworm addition. However, the effects of straw returning combined with earthworm addition on soil ammonia oxidizers remain poorly understood.MethodsA 2-year plot experiment was conducted with 5 treatments: no fertilizer (CK); regular fertilization (RT); straw returning (SR); earthworm addition (W); straw returning + earthworm addition (SRW). The AOA, AOB, comammox clade-A and clade-B community microbial diversities and structures were investigated by high-throughput sequencing.ResultsThe results showed that (1) compared to RT treatment, W, SR, and SRW treatments all significantly increased the richness of AOA and comammox clade-A and clade-B (p < 0.05), and the richness of AOB was only significantly promoted by SRW treatment (p < 0.05). However, only SRW had a higher comammox clade-B diversity index than RT. (2) The ammonia oxidizer community structures were altered by both straw returning and earthworm addition. Soil NH4 +-N was the critical environmental driver for altering the ammonia oxidizer community structure. (3) Compared with RT treatment, the soil potential nitrification rate (PNR) of W and SRW treatments increased by 1.19 and 1.20 times, respectively. The PNR was significantly positively correlated with AOB abundance (path coefficient = 0.712, p < 0.05) and negatively correlated with clade-B abundance (path coefficient = -0.106, p < 0.05).DiscussionThis study provides scientific support for the application of straw returning combined with earthworm addition to improve soil nitrification with respect to soil ammonia-oxidizing microorganisms.

Project description: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 (13)C-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 (13)CO2 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 (13)C-AOB in the JD soil was affiliated with the Nitrosomona communis lineage. The (13)C-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.

Project description:Flooded rice fields are not only a global food source but also a major biogenic source of atmospheric methane. Using metatranscriptomics, we comparatively explored structural and functional succession of paddy soil microbiomes in the oxic surface layer and anoxic bulk soil. Cyanobacteria, Fungi, Xanthomonadales, Myxococcales, and Methylococcales were the most abundant and metabolically active groups in the oxic zone, while Clostridia, Actinobacteria, Geobacter, Anaeromyxobacter, Anaerolineae, and methanogenic archaea dominated the anoxic zone. The protein synthesis potential of these groups was about 75% and 50% of the entire community capacity, respectively. Their structure-function relationships in microbiome succession were revealed by classifying the protein-coding transcripts into core, non-core, and taxon-specific transcripts based on homologous gene distribution. The differential expression of core transcripts between the two microbiomes indicated that structural succession is primarily governed by the cellular ability to adapt to the given oxygen condition, involving oxidative stress, nitrogen/phosphorus metabolism, and fermentation. By contrast, the non-core transcripts were expressed from genes involved in the metabolism of various carbon sources. Among those, taxon-specific transcripts revealed highly specialized roles of the dominant groups in community-wide functioning. For instance, taxon-specific transcripts involved in photosynthesis and methane oxidation were a characteristic of the oxic zone, while those related to methane production and aromatic compound degradation were specific to the anoxic zone. Degradation of organic matters, antibiotics resistance, and secondary metabolite production were detected to be expressed in both the oxic and anoxic zones, but by different taxonomic groups. Cross-feeding of methanol between members of the Methylococcales and Xanthomonadales was suggested by the observation that in the oxic zone, they both exclusively expressed homologous genes encoding methanol dehydrogenase. Our metatranscriptomic analysis suggests that paddy soil microbiomes act as complex, functionally coordinated assemblages whose taxonomic composition is governed by the prevailing habitat factors and their hierarchical importance for community succession.

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Phylogenetically distinct phylotypes modulate nitrification in a paddy soil.

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Phylogenetically distinct phylotypes modulate nitrification in a paddy soil.

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