Succession and community composition of ammonia-oxidizing archaea and bacteria in bulk soil of a Japanese paddy field

Fujii, Chiiho; Nakagawa, Tatsunori; Onodera, Yuki; Matsutani, Naoki; Sasada, Katsuhiro; Takahashi, Reiji; Tokuyama, Tatsuaki

doi:10.1111/j.1747-0765.2010.00449.x

Cited by 30 publications

(19 citation statements)

References 43 publications

(102 reference statements)

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“…The amoA sequences of the strain in AOA-DW were 98.2 to 98.5% identical to those of clones from the sediment of Lakes Acton, Delaware, and Pleasant Hill (C. Li and A. Bollmann, unpublished), 98.5% identical to those of clones from the freshwater sediment in the San Francisco Bay (38), and 98.1% identical to those of clones from a drinking water distribution system in The Netherlands (59). The amoA sequences of the strain in AOA-AC5 were 99% identical to the amoA sequence of a clone from a paddy soil in Japan (18). The strain in the third enrichment culture, AOA-AC2, is closely related to "Ca.…”

Section: Resultsmentioning

confidence: 76%

Ecophysiological Characterization of Ammonia-Oxidizing Archaea and Bacteria from Freshwater

French

Kozlowski

Mukherjee

et al. 2012

Appl Environ Microbiol

176

141

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bAerobic biological ammonia oxidation is carried out by two groups of microorganisms, ammonia-oxidizing bacteria (AOB) and the recently discovered ammonia-oxidizing archaea (AOA). Here we present a study using cultivation-based methods to investigate the differences in growth of three AOA cultures and one AOB culture enriched from freshwater environments. The strain in the enriched AOA culture belong to thaumarchaeal group I.1a, with the strain in one enrichment culture having the highest identity with "Candidatus Nitrosoarchaeum koreensis" and the strains in the other two representing a new genus of AOA. The AOB strain in the enrichment culture was also obtained from freshwater and had the highest identity to AOB from the Nitrosomonas oligotropha group (Nitrosomonas cluster 6a). We investigated the influence of ammonium, oxygen, pH, and light on the growth of AOA and AOB. The growth rates of the AOB increased with increasing ammonium concentrations, while the growth rates of the AOA decreased slightly. Increasing oxygen concentrations led to an increase in the growth rate of the AOB, while the growth rates of AOA were almost oxygen insensitive. Light exposure (white and blue wavelengths) inhibited the growth of AOA completely, and the AOA did not recover when transferred to the dark. AOB were also inhibited by blue light; however, growth recovered immediately after transfer to the dark. Our results show that the tested AOB have a competitive advantage over the tested AOA under most conditions investigated. Further experiments will elucidate the niches of AOA and AOB in more detail. N itrification, the microbial oxidation of NH 3 (ammonia) to NO 3 Ϫ (nitrate), is one of the key processes of the global nitrogen cycle. The first and rate-limiting step of nitrification is the oxidation of NH 3 to NO 2 Ϫ (nitrite). Until recently, aerobic ammonia oxidation was attributed to only a small subset of the Proteobacteria; most freshwater and terrestrial ammonia-oxidizing bacteria (AOB) belong to a distinct group in the Betaproteobacteria, while a few marine AOB species belong to the Gammaproteobacteria (29,32,33). The AOB have a chemolithoautotrophic metabolism, oxidizing NH 3 to NO 2 Ϫ via the intermediate NH 2 OH (hydroxylamine) and fixing carbon from CO 2 (carbon dioxide) via the Calvin cycle (1).Recently, genes encoding ammonia monooxygenase (amoA), the first enzyme in the process of ammonia oxidation, were discovered together with archaeal 16S rRNA genes in a metagenomic study (60) and a soil fosmid library (57). At the same time, Nitrosopumilus maritimus, the first archaeal ammonia oxidizer, was isolated in pure culture from a saltwater aquarium (30). Ammoniaoxidizing archaea (AOA) in pure and enrichment cultures have essentiallythesamemetabolismasAOB;theyoxidizeNH 3 stoichiometrically to NO 2 Ϫ and fix carbon from bicarbonate (HCO 3 Ϫ ) (15,20,30,36,43,56). However, the genomes of N. maritimus and "Candidatus Nitrosoarchaeum limnia" revealed differences between AOA and AOB, such as the use of the 3-hydroxypropionat...

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Section: Resultsmentioning

confidence: 76%

Ecophysiological Characterization of Ammonia-Oxidizing Archaea and Bacteria from Freshwater

French

Kozlowski

Mukherjee

et al. 2012

Appl Environ Microbiol

176

141

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“…Paddy soil represents a special habirat wherein NH^-oxidizing communities are simultaneously shaped by flooding and fertilization. A recent study indicated that the abundance of AOA and AOB varies gready during the rice cultivation period (Fujii et al, 2010); however, the differential response of AOA and AOB community structures to long-term fertilization in paddy soils has not been fully addressed under in situ conditions. A long-term field fertilization experiment can serve as a model system to understand how anthropogenic disturbance may lead to changes in the soil NH^""" concentration, which in turn affects the AOA and AOB community structures under in situ conditions.…”

Section: Agriculturementioning

confidence: 99%

Long‐Term Field Fertilization Significantly Alters Community Structure of Ammonia‐Oxidizing Bacteria rather than Archaea in a Paddy Soil

Wang

et al. 2011

Soil Science Soc of Amer J

124

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Long-term field fertilizarion experiments may provide useful insight into the relative contributions of NHj-oxidizing bacteria (AOB) and NH,-oxidizing archaea (AOA) to soil nitrification. In this study, the abundance and composition of AOB and AOA were investigated in bulk soil from paddy field plots (4 by 5 m) that received no fertilization (CK), 180 kg urea N ha" ' yr" ' (NPK), or 180 kg urea N plus 4500 kg rice [Oryza sativa L.) straw ha"' yr"' (NPK/OM) since 1988 (each with three replicated plots). Our results clearly indicate that long-term fertilization (22 yr) significandy altered the community structure of AOB rather than AOA in the soil within fertilized plots compared with the CK plot. Quantitative polymerase chain reaction analysis of the amoA genes that encode the ammonia monooxygenase subunit A revealed diat the AOB in the fertilized plots were 50 times more abundant than in the CK plot. Denaturing gradient gel electrophoresis fingerprinting of the amoA genes demonstrated a drastic shift in the AOB community structure, resulting in highly enriched AOB similar to Nitrosospira cluster 3 in the fertilized plots. In contrast, the population size and composition of the AOA community remained largely unchanged in all plots. Furthermore, a positive correlation was observed between the bacterial rather than archaeal amoA gene copy numbers and potential nitrification activity among the soils. The distinct responses of AOA and AOB to long-term field fertilization were probably related to the availability of NH,. Our results suggest that AOB might play major roles in the NHj oxidation that occurs in bulk soil under the in situ fertilized paddy field conditions tested in this study.

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“…For a long time, it was believed that only AOB possess the amoA gene for ammonia monooxygenase, the key enzyme of ammonia oxidation (Rotthauwe et al 1997). The occurrence of AOB has been investigated in the flooding paddy soils, including surface soil, rhizosphere, and bulk soil, based on the amoA gene (Briones et al 2002;Nicolaisen et al 2004;Bowatte et al 2006Bowatte et al , 2007Chen et al 2008;Wang et al 2009;Chu et al 2010;Fujii et al 2010). Many studies indicate that Nitrosospira are predominant in the paddy soils (Bowatte et al 2006;Chen et al 2008;Chu et al 2010) while Nitrosomonas are prevalent in high-N fertilizer paddy soils or in the surface of rice roots (Briones et al 2002;Nicolaisen et al 2004).…”

Section: Introductionmentioning

confidence: 99%

“…The AOA are widespread in marine and terrestrial environments with high abundance values (Francis et al 2005;Leininger et al 2006;Wuchter et al 2006;He et al 2007;Shen et al 2008;Schauss et al 2009). Several studies also indicated that AOA outnumbered AOB in paddy soils (Chen et al 2008;Wang et al 2009;Fujii et al 2010), but the contribution of AOA to nitrification in the paddy soil is still unclear. Recently, some researchers found that archaea were not important for nitrification in their tested soils (Di et al 2009;Jia and Conrad 2009).…”

Section: Introductionmentioning

confidence: 99%

Abundance and community structure of ammonia-oxidizing archaea and bacteria in an acid paddy soil

et al. 2011

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Nitrification is essential to the nitrogen cycle in paddy soils. However, it is still not clear which group of ammonia-oxidizing microorganisms plays more important roles in nitrification in the paddy soils. The changes in the abundance and composition of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) were investigated by real-time PCR, terminal restriction fragment length polymorphism, and clone library approaches in an acid red paddy soil subjected to long-term fertilization treatments, including treatment without fertilizers (CT); chemical fertilizer nitrogen (N); N and potassium (NK); N and phosphorus (NP); N, P, and K (NPK); and NPK plus recycled crop residues (NPK+C). The AOA population size in NPK+C was higher than those in CT, while minor changes in AOB population sizes were detected among the treatments. There were also some changes in AOA community composition responding to different fertilization treatments. Still few differences were detected in AOB community composition among the treatments. Phylogenetic analysis showed that the AOA sequences fell into two main clusters: cluster A and cluster soil/sediment. The AOB composition in this paddy soil was dominated by Nitrosospira cluster 12. These results suggested that the AOA were more sensitive than AOB to different fertilization treatments in the acid red paddy soil.

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Succession and community composition of ammonia-oxidizing archaea and bacteria in bulk soil of a Japanese paddy field

Cited by 30 publications

References 43 publications

Ecophysiological Characterization of Ammonia-Oxidizing Archaea and Bacteria from Freshwater

Ecophysiological Characterization of Ammonia-Oxidizing Archaea and Bacteria from Freshwater

Long‐Term Field Fertilization Significantly Alters Community Structure of Ammonia‐Oxidizing Bacteria rather than Archaea in a Paddy Soil

Abundance and community structure of ammonia-oxidizing archaea and bacteria in an acid paddy soil

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