Autotrophic growth of nitrifying community in an agricultural soil

The two-step nitrification process is an integral part of the global nitrogen cycle, and it is accomplished by distinctly different nitrifiers. By combining DNA-based stable isotope probing (SIP) and high-throughput pyrosequencing, we present the molecular evidence for autotrophic growth of ammonia-...

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Published in	The ISME Journal Vol. 5; no. 7; pp. 1226 - 1236
Main Authors	Xia, Weiwei, Zhang, Caixia, Zeng, Xiaowei, Feng, Youzhi, Weng, Jiahua, Lin, Xiangui, Zhu, Jianguo, Xiong, Zhengqin, Xu, Jian, Cai, Zucong, Jia, Zhongjun
Format	Journal Article
Language	English
Published	London Nature Publishing Group UK 01.07.2011 Oxford University Press Nature Publishing Group
Subjects	631/326/171/1818 631/326/2565/855 631/443/319 Agricultural land Agriculture Ammonia Ammonia - metabolism Ammonium Archaea - classification Archaea - genetics Archaea - growth & development Autotrophic Processes Bacteria - classification Bacteria - genetics Bacteria - growth & development Biomedical and Life Sciences Carbon dioxide Deoxyribonucleic acid DNA Ecology Evolutionary Biology Gene Library Genes, Archaeal Genes, Bacterial Genes, rRNA High-Throughput Nucleotide Sequencing Hot springs Incubation Life Sciences Microbial Ecology Microbial Genetics and Genomics Microbiology Microcosms Nitrification Nitrites - metabolism Nitrogen cycle Original original-article Oxidation Phylogeny Sequence Analysis, DNA Soil - analysis Soil environment Soil Microbiology Soil testing Soils Stable isotopes ammonia-oxidizing bacteria stable isotope probing pyrosequencing nitrite-oxidizing bacteria agricultural soil ammonia-oxidizing archaea
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Abstract	The two-step nitrification process is an integral part of the global nitrogen cycle, and it is accomplished by distinctly different nitrifiers. By combining DNA-based stable isotope probing (SIP) and high-throughput pyrosequencing, we present the molecular evidence for autotrophic growth of ammonia-oxidizing bacteria (AOB), ammonia-oxidizing archaea (AOA) and nitrite-oxidizing bacteria (NOB) in agricultural soil upon ammonium fertilization. Time-course incubation of SIP microcosms indicated that the amoA genes of AOB was increasingly labeled by 13 CO 2 after incubation for 3, 7 and 28 days during active nitrification, whereas labeling of the AOA amoA gene was detected to a much lesser extent only after a 28-day incubation. Phylogenetic analysis of the 13 C-labeled amoA and 16S rRNA genes revealed that the Nitrosospira cluster 3-like sequences dominate the active AOB community and that active AOA is affiliated with the moderately thermophilic Nitrososphaera gargensis from a hot spring. The higher relative frequency of Nitrospira -like NOB in the 13 C-labeled DNA suggests that it may be more actively involved in nitrite oxidation than Nitrobacter -like NOB. Furthermore, the acetylene inhibition technique showed that 13 CO 2 assimilation by AOB, AOA and NOB occurs only when ammonia oxidation is not blocked, which provides strong hints for the chemolithoautotrophy of nitrifying community in complex soil environments. These results show that the microbial community of AOB and NOB dominates the nitrification process in the agricultural soil tested.
AbstractList	The two-step nitrification process is an integral part of the global nitrogen cycle, and it is accomplished by distinctly different nitrifiers. By combining DNA-based stable isotope probing (SIP) and high-throughput pyrosequencing, we present the molecular evidence for autotrophic growth of ammonia-oxidizing bacteria (AOB), ammonia-oxidizing archaea (AOA) and nitrite-oxidizing bacteria (NOB) in agricultural soil upon ammonium fertilization. Time-course incubation of SIP microcosms indicated that the amoA genes of AOB was increasingly labeled by 13 CO 2 after incubation for 3, 7 and 28 days during active nitrification, whereas labeling of the AOA amoA gene was detected to a much lesser extent only after a 28-day incubation. Phylogenetic analysis of the 13 C-labeled amoA and 16S rRNA genes revealed that the Nitrosospira cluster 3-like sequences dominate the active AOB community and that active AOA is affiliated with the moderately thermophilic Nitrososphaera gargensis from a hot spring. The higher relative frequency of Nitrospira -like NOB in the 13 C-labeled DNA suggests that it may be more actively involved in nitrite oxidation than Nitrobacter -like NOB. Furthermore, the acetylene inhibition technique showed that 13 CO 2 assimilation by AOB, AOA and NOB occurs only when ammonia oxidation is not blocked, which provides strong hints for the chemolithoautotrophy of nitrifying community in complex soil environments. These results show that the microbial community of AOB and NOB dominates the nitrification process in the agricultural soil tested. The two-step nitrification process is an integral part of the global nitrogen cycle, and it is accomplished by distinctly different nitrifiers. By combining DNA-based stable isotope probing (SIP) and high-throughput pyrosequencing, we present the molecular evidence for autotrophic growth of ammonia-oxidizing bacteria (AOB), ammonia-oxidizing archaea (AOA) and nitrite-oxidizing bacteria (NOB) in agricultural soil upon ammonium fertilization. Time-course incubation of SIP microcosms indicated that the amoA genes of AOB was increasingly labeled by (13)CO(2) after incubation for 3, 7 and 28 days during active nitrification, whereas labeling of the AOA amoA gene was detected to a much lesser extent only after a 28-day incubation. Phylogenetic analysis of the (13)C-labeled amoA and 16S rRNA genes revealed that the Nitrosospira cluster 3-like sequences dominate the active AOB community and that active AOA is affiliated with the moderately thermophilic Nitrososphaera gargensis from a hot spring. The higher relative frequency of Nitrospira-like NOB in the (13)C-labeled DNA suggests that it may be more actively involved in nitrite oxidation than Nitrobacter-like NOB. Furthermore, the acetylene inhibition technique showed that (13)CO(2) assimilation by AOB, AOA and NOB occurs only when ammonia oxidation is not blocked, which provides strong hints for the chemolithoautotrophy of nitrifying community in complex soil environments. These results show that the microbial community of AOB and NOB dominates the nitrification process in the agricultural soil tested. The two-step nitrification process is an integral part of the global nitrogen cycle, and it is accomplished by distinctly different nitrifiers. By combining DNA-based stable isotope probing (SIP) and high-throughput pyrosequencing, we present the molecular evidence for autotrophic growth of ammonia-oxidizing bacteria (AOB), ammonia-oxidizing archaea (AOA) and nitrite-oxidizing bacteria (NOB) in agricultural soil upon ammonium fertilization. Time-course incubation of SIP microcosms indicated that the amoA genes of AOB was increasingly labeled by 13CO2 after incubation for 3, 7 and 28 days during active nitrification, whereas labeling of the AOA amoA gene was detected to a much lesser extent only after a 28-day incubation. Phylogenetic analysis of the 13C-labeled amoA and 16S rRNA genes revealed that the Nitrosospira cluster 3-like sequences dominate the active AOB community and that active AOA is affiliated with the moderately thermophilic Nitrososphaera gargensis from a hot spring. The higher relative frequency of Nitrospira-like NOB in the 13C-labeled DNA suggests that it may be more actively involved in nitrite oxidation than Nitrobacter-like NOB. Furthermore, the acetylene inhibition technique showed that 13CO2 assimilation by AOB, AOA and NOB occurs only when ammonia oxidation is not blocked, which provides strong hints for the chemolithoautotrophy of nitrifying community in complex soil environments. These results show that the microbial community of AOB and NOB dominates the nitrification process in the agricultural soil tested. The two-step nitrification process is an integral part of the global nitrogen cycle, and it is accomplished by distinctly different nitrifiers. By combining DNA-based stable isotope probing (SIP) and high-throughput pyrosequencing, we present the molecular evidence for autotrophic growth of ammonia-oxidizing bacteria (AOB), ammonia-oxidizing archaea (AOA) and nitrite-oxidizing bacteria (NOB) in agricultural soil upon ammonium fertilization. Time-course incubation of SIP microcosms indicated that the amoA genes of AOB was increasingly labeled by (13)CO(2) after incubation for 3, 7 and 28 days during active nitrification, whereas labeling of the AOA amoA gene was detected to a much lesser extent only after a 28-day incubation. Phylogenetic analysis of the (13)C-labeled amoA and 16S rRNA genes revealed that the Nitrosospira cluster 3-like sequences dominate the active AOB community and that active AOA is affiliated with the moderately thermophilic Nitrososphaera gargensis from a hot spring. The higher relative frequency of Nitrospira-like NOB in the (13)C-labeled DNA suggests that it may be more actively involved in nitrite oxidation than Nitrobacter-like NOB. Furthermore, the acetylene inhibition technique showed that (13)CO(2) assimilation by AOB, AOA and NOB occurs only when ammonia oxidation is not blocked, which provides strong hints for the chemolithoautotrophy of nitrifying community in complex soil environments. These results show that the microbial community of AOB and NOB dominates the nitrification process in the agricultural soil tested.The two-step nitrification process is an integral part of the global nitrogen cycle, and it is accomplished by distinctly different nitrifiers. By combining DNA-based stable isotope probing (SIP) and high-throughput pyrosequencing, we present the molecular evidence for autotrophic growth of ammonia-oxidizing bacteria (AOB), ammonia-oxidizing archaea (AOA) and nitrite-oxidizing bacteria (NOB) in agricultural soil upon ammonium fertilization. Time-course incubation of SIP microcosms indicated that the amoA genes of AOB was increasingly labeled by (13)CO(2) after incubation for 3, 7 and 28 days during active nitrification, whereas labeling of the AOA amoA gene was detected to a much lesser extent only after a 28-day incubation. Phylogenetic analysis of the (13)C-labeled amoA and 16S rRNA genes revealed that the Nitrosospira cluster 3-like sequences dominate the active AOB community and that active AOA is affiliated with the moderately thermophilic Nitrososphaera gargensis from a hot spring. The higher relative frequency of Nitrospira-like NOB in the (13)C-labeled DNA suggests that it may be more actively involved in nitrite oxidation than Nitrobacter-like NOB. Furthermore, the acetylene inhibition technique showed that (13)CO(2) assimilation by AOB, AOA and NOB occurs only when ammonia oxidation is not blocked, which provides strong hints for the chemolithoautotrophy of nitrifying community in complex soil environments. These results show that the microbial community of AOB and NOB dominates the nitrification process in the agricultural soil tested.
Author	Zhu, Jianguo Cai, Zucong Jia, Zhongjun Weng, Jiahua Lin, Xiangui Xiong, Zhengqin Xu, Jian Zhang, Caixia Xia, Weiwei Zeng, Xiaowei Feng, Youzhi
Author_xml	– sequence: 1 givenname: Weiwei surname: Xia fullname: Xia, Weiwei organization: State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, China, Graduate School of the Chinese Academy of Sciences – sequence: 2 givenname: Caixia surname: Zhang fullname: Zhang, Caixia organization: College of Resources and Environmental Sciences, Nanjing Agricultural University – sequence: 3 givenname: Xiaowei surname: Zeng fullname: Zeng, Xiaowei organization: BioEnergy Genome Center, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences – sequence: 4 givenname: Youzhi surname: Feng fullname: Feng, Youzhi organization: State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, China – sequence: 5 givenname: Jiahua surname: Weng fullname: Weng, Jiahua organization: State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, China – sequence: 6 givenname: Xiangui surname: Lin fullname: Lin, Xiangui organization: State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, China – sequence: 7 givenname: Jianguo surname: Zhu fullname: Zhu, Jianguo organization: State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, China – sequence: 8 givenname: Zhengqin surname: Xiong fullname: Xiong, Zhengqin organization: College of Resources and Environmental Sciences, Nanjing Agricultural University – sequence: 9 givenname: Jian surname: Xu fullname: Xu, Jian organization: BioEnergy Genome Center, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences – sequence: 10 givenname: Zucong surname: Cai fullname: Cai, Zucong organization: State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, China – sequence: 11 givenname: Zhongjun surname: Jia fullname: Jia, Zhongjun email: jia@issas.ac.cn organization: State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, China
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/21326337$$D View this record in MEDLINE/PubMed
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Snippet	The two-step nitrification process is an integral part of the global nitrogen cycle, and it is accomplished by distinctly different nitrifiers. By combining...
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SubjectTerms	631/326/171/1818 631/326/2565/855 631/443/319 Agricultural land Agriculture Ammonia Ammonia - metabolism Ammonium Archaea - classification Archaea - genetics Archaea - growth & development Autotrophic Processes Bacteria - classification Bacteria - genetics Bacteria - growth & development Biomedical and Life Sciences Carbon dioxide Deoxyribonucleic acid DNA Ecology Evolutionary Biology Gene Library Genes, Archaeal Genes, Bacterial Genes, rRNA High-Throughput Nucleotide Sequencing Hot springs Incubation Life Sciences Microbial Ecology Microbial Genetics and Genomics Microbiology Microcosms Nitrification Nitrites - metabolism Nitrogen cycle Original original-article Oxidation Phylogeny Sequence Analysis, DNA Soil - analysis Soil environment Soil Microbiology Soil testing Soils Stable isotopes
Title	Autotrophic growth of nitrifying community in an agricultural soil
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