Competitive interactions between methane- and ammonia-oxidizing bacteria modulate carbon and nitrogen cycling in paddy soil

Yan Zheng, Rong Huang, B. Wang, P.L.E. Bodelier, Z. Jia

Research output: Contribution to journal/periodicalArticleScientificpeer-review

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Pure culture studies have demonstrated that methanotrophs and ammonia oxidizers can both carry out the oxidation of methane and ammonia. However, the expected interactions resulting from these similarities are poorly understood, especially in complex, natural environments. Using DNA-based stable isotope probing and pyrosequencing of 16S rRNA and pmoA genes, we report on biogeochemical and molecular evidence for growth stimulation of methanotrophic communities by ammonium fertilization, and that methane modulates nitrogen cycling by competitive inhibition of nitrifying communities in a rice paddy soil. Pairwise comparison between microcosms amended with CH4, CH4+Urea, and Urea indicated that urea fertilization stimulated methane oxidation activity by 6-fold during a 19 day incubation period, while ammonia oxidation activity was significantly inhibited in the presence of CH4. Pyrosequencing of the total 16S rRNA genes revealed that urea amendment resulted in rapid growth of Methylosarcina-like type Ia MOB, and nitrifying communities appeared to be suppressed by methane. High-throughput sequencing of the 13C-labeled DNA further revealed that methane amendment resulted in clear growth of Methylosarcina-related MOB while methane plus urea led to equal increase in Methylosarcina and Methylobacter-related MOB, indicating the differential growth requirements of representatives of these genera. Strikingly, type Ib MOB did not respond to methane nor to urea. Increase in 13C-assimilation by microorganisms related to methanol oxidizers clearly indicated carbon transfer from methane oxidation to other soil microbes, which was enhanced by urea addition. The active growth of type Ia methanotrops was significantly stimulated by urea amendment, and the pronounced growth of methanol-oxidizing bacteria occurred in CH4-treated microcosms only upon urea amendment. Methane addition inhibited the growth of Nitrosospira and Nitrosomonas in urea-amended microcosms, in addition of nitrite-oxidizing bacteria. These results provide comprehensive insights in the interactions between actively growing methanotrophs and ammonia oxidizers in a complex soil ecosystem.
Original languageEnglish
Pages (from-to)3353-3368
Publication statusPublished - 2014


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