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Interactions between Thaumarchaea, Nitrospira and methanotrophs modulate autotrophic nitrification in volcanic grassland soil.

ABSTRACT: Ammonium/ammonia is the sole energy substrate of ammonia oxidizers, and is also an essential nitrogen source for other microorganisms. Ammonia oxidizers therefore must compete with other soil microorganisms such as methane-oxidizing bacteria (MOB) in terrestrial ecosystems when ammonium concentrations are limiting. Here we report on the interactions between nitrifying communities dominated by ammonia-oxidizing archaea (AOA) and Nitrospira-like nitrite-oxidizing bacteria (NOB), and communities of MOB in controlled microcosm experiments with two levels of ammonium and methane availability. We observed strong stimulatory effects of elevated ammonium concentration on the processes of nitrification and methane oxidation as well as on the abundances of autotrophically growing nitrifiers. However, the key players in nitrification and methane oxidation, identified by stable-isotope labeling using (13)CO2 and (13)CH4, were the same under both ammonium levels, namely type 1.1a AOA, sublineage I and II Nitrospira-like NOB and Methylomicrobium-/Methylosarcina-like MOB, respectively. Ammonia-oxidizing bacteria were nearly absent, and ammonia oxidation could almost exclusively be attributed to AOA. Interestingly, although AOA functional gene abundance increased 10-fold during incubation, there was very limited evidence of autotrophic growth, suggesting a partly mixotrophic lifestyle. Furthermore, autotrophic growth of AOA and NOB was inhibited by active MOB at both ammonium levels. Our results suggest the existence of a previously overlooked competition for nitrogen between nitrifiers and methane oxidizers in soil, thus linking two of the most important biogeochemical cycles in nature.

SUBMITTER: Daebeler A

PROVIDER: S-EPMC4260704 | biostudies-literature | 2014 Dec

REPOSITORIES: biostudies-literature

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Interactions between Thaumarchaea, Nitrospira and methanotrophs modulate autotrophic nitrification in volcanic grassland soil.

Daebeler Anne A Bodelier Paul L E PL Yan Zheng Z Hefting Mariet M MM Jia Zhongjun Z Laanbroek Hendrikus J HJ

The ISME journal 20140523 12

Ammonium/ammonia is the sole energy substrate of ammonia oxidizers, and is also an essential nitrogen source for other microorganisms. Ammonia oxidizers therefore must compete with other soil microorganisms such as methane-oxidizing bacteria (MOB) in terrestrial ecosystems when ammonium concentrations are limiting. Here we report on the interactions between nitrifying communities dominated by ammonia-oxidizing archaea (AOA) and Nitrospira-like nitrite-oxidizing bacteria (NOB), and communities of ...[more]

PMID: 24858784

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Project description:The effect of different cropping systems on CO2 fixation by soil microorganisms was studied by comparing soils from three exemplary cropping systems after 10 years of agricultural practice. Studied cropping systems included: continuous cropping of paddy rice (rice-rice), rotation of paddy rice and rapeseed (rice-rapeseed), and rotated cropping of rapeseed and corn (rapeseed-corn). Soils from different cropping systems were incubated with continuous (14)C-CO2 labeling for 110 days. The CO2-fixing bacterial communities were investigated by analyzing the cbbL gene encoding ribulose-1,5-bisphosphate carboxylase oxygenase (RubisCO). Abundance, diversity and activity of cbbL-carrying bacteria were analyzed by quantitative PCR, cbbL clone libraries and enzyme assays. After 110 days incubation, substantial amounts of (14)C-CO2 were incorporated into soil organic carbon ((14)C-SOC) and microbial biomass carbon ((14)C-MBC). Rice-rice rotated soil showed stronger incorporation rates when looking at (14)C-SOC and (14)C-MBC contents. These differences in incorporation rates were also reflected by determined RubisCO activities. (14)C-MBC, cbbL gene abundances and RubisCO activity were found to correlate significantly with (14)C-SOC, indicating cbbL-carrying bacteria to be key players for CO2 fixation in these soils. The analysis of clone libraries revealed distinct cbbL-carrying bacterial communities for the individual soils analyzed. Most of the identified operational taxonomic units (OTU) were related to Nitrobacter hamburgensis, Methylibium petroleiphilum, Rhodoblastus acidophilus, Bradyrhizobium, Cupriavidus metallidurans, Rubrivivax, Burkholderia, Stappia, and Thiobacillus thiophilus. OTUs related to Rubrivivax gelatinosus were specific for rice-rice soil. OTUs linked to Methylibium petroleiphilum were exclusively found in rice-rapeseed soil. Observed differences could be linked to differences in soil parameters such as SOC. We conclude that the long-term application of cropping systems alters underlying soil parameters, which in turn selects for distinct autotrophic communities.

Project description:Enclosure and grazing can significantly change the turnover of nitrogen in grassland soil. Changes of soil nitrogen mineralization and ammonium-oxidizing microorganisms caused by enclosure in different grazing intensities (about 30 years of grazing history) grassland, however, has rarely been reported. We selected the grassland sites with high and medium grazing intensity (HG and MG, 4 and 2 sheep ha-1, respectively) and had them enclosed (45 × 55 m) in 2005 while outside the enclosure was continuously grazed year-round. A two factorial study was designed: grazing intensity (MG and HG sites) and enclosure (fence and non-fence). Nitrogen mineralization was detected through a laboratory incubation experiment. The abundance and community structure of soil ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB) were analyzed using quantitative PCR (q-PCR), terminal-restriction fragment length polymorphism (T-RFLP), cloning, and sequencing. Results showed that compared with MG site, at HG site the AOB abundance and community structure of AOB changed significantly while the AOA abundance and community structure did not change obviously. Enclosure significantly decreased the cumulative mineralized N, N mineralization rate, the abundance of AOB and the AOB community structure at the HG site, while at MG site, enclosure did not change these parameters. Potential nitrification rate (PNR) was positively correlated with the abundance of AOA and AOB at the MG and HG sites, respectively. The abundance of AOA was significantly correlated with soil pH; however, AOB abundance was significantly correlated with soil available N, total N, C/N ratio, pH, etc. The phylogenetic analysis showed that Nitrososphaeraceae and Nitrosomonadaceae were the dominant AOA and AOB, respectively. Totally, the responses of AOB and AOA mainly were associated to changes in soil physicochemical properties caused by different intensity grazing; AOB and AOA may be the dominant functional players in ammonia oxidation processes at HG and MG site, respectively.

Dataset Information

Interactions between Thaumarchaea, Nitrospira and methanotrophs modulate autotrophic nitrification in volcanic grassland soil.

Publications

Interactions between Thaumarchaea, Nitrospira and methanotrophs modulate autotrophic nitrification in volcanic grassland soil.

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