Potential Contribution of Anammox to Nitrogen Loss from Paddy Soils in Southern China

Yang, Xiao-Ru; Li, Hu; Nie, Shuang; Su, Jian‐Qiang; Weng, Bosen; Zhu, Guibing; Yao, Huaiying; Gilbert, Jack A.; Zhu, Yan

doi:10.1128/aem.02664-14

Cited by 127 publications

(109 citation statements)

References 52 publications

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“…Similar to previous reports, Candidatus Brocadia dominated in this paddy soils fields (Bai et al, 2015;Yang et al, 2015). Bacteria of this genus harbor diverse metabolism (Gori et al, 2011), with the ability to use short-chain organic acids as electron donors instead of NH 4 þ , making it highly adaptable.…”

Section: Discussionsupporting

confidence: 65%

“…Agricultural fields with intensive application of mineral fertilizers have been reported as ideal habitats for anammox bacteria Yang et al, 2015). Broad distribution of diverse anammox bacteria has been detected in agricultural soils (Zhu et al, 2011a;Shen et al, 2013;Wang and Gu, 2013), and a considerable proportion of N 2 production in paddy soils in Southern China could be attributed to the anammox process based on incubation studies .…”

Section: Introductionmentioning

confidence: 97%

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The phenological stage of rice growth determines anaerobic ammonium oxidation activity in rhizosphere soil

Yang

Weng

et al. 2016

Soil Biology and Biochemistry

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a b s t r a c tAnaerobic oxidation of ammonium (anammox) plays an important role in nitrogen (N) loss from agricultural systems. Recently, the rice rhizosphere was demonstrated to be a hotspot for anammox, yet the dynamics of anammox activity and the distribution of anammox bacteria in rhizosphere soil at different phenological stages of rice growth are still unknown. In this study, the activity, diversity and abundance of anammox bacteria in both rhizosphere and bulk soils were investigated over the entire rice growth season. From tillering to ripening stage, significantly higher anammox bacterial abundance was detected in rhizosphere soils compared to bulk soils. The rhizosphere soils also had significantly higher anammox rates at tillering and booting stages (0.71 and 0.32 nmol N g À1 dry soil h À1 , respectively) compared to bulk soils. The anammox rate in rhizosphere soil was positively correlated to the concentrations of NO x À (total of nitrate and nitrite) and acetate. The abundance of anammox bacteria was significantly correlated with the concentration of succinate in rhizosphere soils. A total of five anammox genera of Brocadia, Kuenenia, Anammoxoglobus, Jettenia and Scalindua were detected, with Brocadia predominating in all examined samples. The distribution of anammox bacteria in rhizosphere and bulk soils varied with phenological stages. Statistical analysis indicated that C/N ratio, formate, citrate and ammonium were key factors influencing the composition of anammox bacteria. Variations in activity, abundance and distribution of anammox bacteria in rhizosphere were observed over the phenological progression, demonstrating that the root exudates might be influential for the anammox process. This study implies that future efforts in estimating the rate of anammox should consider the temporal variation during plant life cycles.

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Section: Discussionsupporting

confidence: 65%

Section: Introductionmentioning

confidence: 97%

The phenological stage of rice growth determines anaerobic ammonium oxidation activity in rhizosphere soil

Yang

Weng

et al. 2016

Soil Biology and Biochemistry

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“…The columns in the box chart represent the log number of the hzsB gene copy (copies g −1 dry soil). For all boxplots, black center lines represent the median and box edges are the first and third quartiles comparable to that reported in rivers (Zhao et al 2013), lakes (Schubert et al 2006;Wenk et al 2014), paddy soils (Zhu et al 2011;Yang et al 2015), and other estuaries (RisgaardPetersen et al 2004;Rysgaard et al 2004;Engström et al 2005), but lower than that generally detected in marine ecosystems (Tamdrup and Dalsgaard 2002;Brabandere et al 2014). Based on our results, N loss attributed to anammox was estimated to reach an average value of 9.70 × 10 5 t N per year on the basis of sediment weight, study area, and anammox average rate obtained from slurry incubations.…”

Section: Discussionmentioning

confidence: 90%

“…Heterotrophic denitrification was considered to be the only known pathway for the loss of fixed nitrogen to the atmosphere for decades until the discovery of anammox bacteria in a wastewater treatment plant (Mulder et al 1995). Subsequently, anammox bacteria were detected with broad biogeographic distribution in various natural ecosystems, including marine sediments (Thamdrup and Dalsgaard 2002;Trimmer and Nicholls 2009;Brabandere et al 2014;Shao et al 2014;Dang et al 2016), estuarine sediments (Dale et al 2009;Dang et al 2010;Li et al 2011;Wang et al 2012a, b;Dang et al 2013), and paddy soils (Zhu et al 2011;Nie et al 2015;Yang et al 2015). The relative contribution of anammox to dinitrogen production can vary widely, with >80% of total N 2 production observed in the eastern tropical South Pacific oxygen minimum zone (OMZ) off the coast of northern Chile (Brabandere et al 2014).…”

Section: Electronic Supplementary Materialsmentioning

confidence: 99%

“…The anammox genotype is associated with hydrazine synthase, an intermediate step in the anammox pathway that synthesizes hydrazine from nitric oxide and ammonium . We used the hzsB gene that encodes one of the hydrazine synthase subunits as a molecular marker (Wang et al 2012a, b;Zhu et al 2013;Yang et al 2015) in order to determine the abundance and diversity of anammox bacteria.…”

Section: Electronic Supplementary Materialsmentioning

confidence: 99%

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An overlooked nitrogen loss linked to anaerobic ammonium oxidation in estuarine sediments in China

Yang

Weng

et al. 2017

J Soils Sediments

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Purpose Despite its importance, anammox (anaerobic ammonium oxidation) in estuarine sediment systems remains poorly understood, particularly at the continental scale. This study aimed to understand the abundance, diversity, and activity of anammox bacteria and to determine the main factors influencing the anammox process in estuarine sediments in China. Materials and methods Estuarine sediments were collected from 18 estuaries spanning over 4000 km. Experiments using an 15 N-tracer, quantitative PCR, and clone library construction were used to determine the activity, abundance, and diversity of anammox bacteria. The impact of environmental factors on anammox processes was also determined.Results and discussion The abundance of the anammoxspecific hydrazine synthase (hzsB) gene ranged from 1.8 × 10 5 ± 3.4 × 10 4 to 3.6 × 10 8 ± 7.5 × 10 7 copies g −1 dw. Candidatus Scalindua, Brocadia, Kuenenia, Jettenia, and two novel unidentified clusters were detected, with Scalindua dominating the anammox population. Additionally, the abundances of Scalindua, Kuenenia, and Brocadia were found to be significantly correlated with latitude. The anammox rates ranged from 0.29 ± 0.15 to 13.68 ± 3.98 nmol N g −1 dw h −1 and contributed to 2.39-82.61% of total N 2 production. Pearson correlation analysis revealed that the anammox rate was positively correlated with total nitrogen, total carbon, and temperature, and was negatively correlated with dissolved oxygen (DO). The key factors influencing the hzsB gene abundance were ammonium concentration, salinity, and DO. Ammonium concentration, pH, temperature, and latitude were main variables shaping the anammox-associated bacterial community. Conclusions Our results suggested that anammox bacteria are ubiquitous in coastal estuaries in China and underline the importance of anammox resulting in N loss at a continental scale.

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High‐throughput analysis of anammox bacteria in wetland and dryland soils along the altitudinal gradient in Qinghai–Tibet Plateau

et al. 2017

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This study investigated the diversity, community composition, and abundance of anaerobic ammonium oxidation (anammox) bacteria along the altitudinal gradient in Qinghai–Tibet Plateau. Two types of soil samples (wetland and dryland soils, n = 123) were collected from 641 m to 5,033 m altitudes. Polymerase chain reaction (PCR) screening showed that anammox were not widespread, and were only detected in 9 sampling sites of the 50 sites tested by amplifying the 16S rRNA genes. Then, only samples collected from Linzhi (2,715 m), Rikaze (4,030 m), and Naqu (5,011 m), which were positive for the presence of anammox, were further processed to explore the biogeography of anammox bacteria in Qinghai–Tibet Plateau. Results of high‐throughput sequencing targeting the hydrazine synthesis β‐subunit (hzsB) gene revealed the presence of three known anammox genera (Candidatus Brocadia, Candidatus Jettenia, and Candidatus Kuenenia) in both soil types. Their diversity, community composition, and abundance did not show significant variation with altitude at large scale. However, it was the small‐scale environmental heterogeneities between wetland and dryland soils that determined their biogeographical distribution. Specifically, the dryland soils had higher diversity of anammox bacteria than the wetland soils, but their abundance patterns varied. The community composition of anammox bacteria were found to be influenced by soil nitrate content.

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Potential Contribution of Anammox to Nitrogen Loss from Paddy Soils in Southern China

Cited by 127 publications

References 52 publications

The phenological stage of rice growth determines anaerobic ammonium oxidation activity in rhizosphere soil

The phenological stage of rice growth determines anaerobic ammonium oxidation activity in rhizosphere soil

An overlooked nitrogen loss linked to anaerobic ammonium oxidation in estuarine sediments in China

High‐throughput analysis of anammox bacteria in wetland and dryland soils along the altitudinal gradient in Qinghai–Tibet Plateau

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