Cited by 225Soil Carbon and Nitrogen DynamicsWastewater Treatment and Nitrogen RemovalMicrobial Community Ecology and Physiology

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

Differential contributions of ammonia oxidizers and nitrite oxidizers to nitrification in four paddy soils

Open access

Abstract

Rice paddy fields are characterized by regular flooding and nitrogen fertilization, but the functional importance of aerobic ammonia oxidizers and nitrite oxidizers under unique agricultural management is poorly understood. In this study, we report the differential contributions of ammonia-oxidizing archaea (AOA), bacteria (AOB) and nitrite-oxidizing bacteria (NOB) to nitrification in four paddy soils from different geographic regions (Zi-Yang (ZY), Jiang-Du (JD), Lei-Zhou (LZ) and Jia-Xing (JX)) that are representative of the rice ecosystems in China. In urea-amended microcosms, nitrification activity varied greatly with 11.9, 9.46, 3.03 and 1.43 μg NO3−-N g−1 dry weight of soil per day in the ZY, JD, LZ and JX soils, respectively, over the course of a 56-day incubation period. Real-time quantitative PCR of amoA genes and pyrosequencing of 16S rRNA genes revealed significant increases in the AOA population to various extents, suggesting that their relative contributions to ammonia oxidation activity decreased from ZY to JD to LZ. The opposite trend was observed for AOB, and the JX soil stimulated only the AOB populations. DNA-based stable-isotope probing further demonstrated that active AOA numerically outcompeted their bacterial counterparts by 37.0-, 10.5- and 1.91-fold in 13C-DNA from ZY, JD and LZ soils, respectively, whereas AOB, but not AOA, were labeled in the JX soil during active nitrification. NOB were labeled to a much greater extent than AOA and AOB, and the addition of acetylene completely abolished the assimilation of 13CO2 by nitrifying populations. Phylogenetic analysis suggested that archaeal ammonia oxidation was predominantly catalyzed by soil fosmid 29i4-related AOA within the soil group 1.1b lineage. Nitrosospira cluster 3-like AOB performed most bacterial ammonia oxidation in the ZY, LZ and JX soils, whereas the majority of the 13C-AOB in the JD soil was affiliated with the Nitrosomona communis lineage. The 13C-NOB was overwhelmingly dominated by Nitrospira rather than Nitrobacter. A significant correlation was observed between the active AOA/AOB ratio and the soil oxidation capacity, implying a greater advantage of AOA over AOB under microaerophilic conditions. These results suggest the important roles of soil physiochemical properties in determining the activities of ammonia oxidizers and nitrite oxidizers.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/ismej.2014.194

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 59

  1. Alonso-Sáez, 2012, Role for urea in nitrification by polar marine Archaea, Proc Natl Acad Sci USA, 109, 17989, 10.1073/pnas.1201914109 · DOI
  2. Alves, 2013, Nitrification rates in Arctic soils are associated with functionally distinct populations of ammonia-oxidizing archaea, ISME J, 7, 1620, 10.1038/ismej.2013.35 · DOI
  3. Bannert, 2011, Comparison of lipid biomarker and gene abundance characterizing the archaeal ammonia-oxidizing community in flooded soils, Biol Fertil Soils, 47, 839, 10.1007/s00374-011-0552-6 · DOI
  4. Bates, 2011, Examining the global distribution of dominant archaeal populations in soil, ISME J, 5, 908, 10.1038/ismej.2010.171 · DOI
  5. Belser, 1984, Bicarbonate uptake by nitrifiers: effects of growth rate, pH, substrate concentration, and metabolic inhibitors, Appl Environ Microbiol, 48, 1100, 10.1128/aem.48.6.1100-1104.1984 · DOI
  6. Berg, 1982, Inhibitory effect of low partial pressures of acetylene on nitrification, Soil Biol Biochem, 14, 301, 10.1016/0038-0717(82)90041-4 · DOI
  7. Bock, 2006, The Prokaryotes, 457, 10.1007/0-387-30742-7_16 · DOI
  8. Chen, 2008, Ammonia-oxidizing archaea: important players in paddy rhizosphere soil?, Environ Microbiol, 10, 1978, 10.1111/j.1462-2920.2008.01613.x · DOI
  9. Clarke, 1993, A method of linking multivariate community structure to environmental variables, Mar Ecol Prog Ser, 92, 205, 10.3354/meps092205 · DOI
  10. Daims, 2001, In situ characterization of Nitrospira-like nitrite-oxidizing bacteria active in wastewater treatment plants, Appl Environ Microbiol, 67, 5273, 10.1128/AEM.67.11.5273-5284.2001 · DOI
  11. 10.1111/1462-2920.12367 · DOI
  12. Ehrich, 1995, A new obligately chemolithoautotrophic, nitrite-oxidizing bacterium, Nitrospira moscoviensis sp. nov. and its phylogenetic relationship, Arch Microbiol, 164, 16, 10.1007/BF02568729 · DOI
  13. Feliatra, 1993, Rates of nitrification and carbon uptake in the Rhone River plume (northwestern Mediterranean Sea), Microb Ecol, 26, 21, 10.1007/BF00166026 · DOI
  14. Food and Agricultural Organization of the United Nations (FAO), 2014, Statistics Division of the Food and Agricultural Organization of the United Nations (FAOSTAT)
  15. Francis, 2005, Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean, Proc Natl Acad Sci USA, 102, 14683, 10.1073/pnas.0506625102 · DOI
  16. Freitag, 2006, Changes in the community structure and activity of betaproteobacterial ammonia-oxidizing sediment bacteria along a freshwater-marine gradient, Environ Microbiol, 8, 684, 10.1111/j.1462-2920.2005.00947.x · DOI
  17. French, 2012, Ecophysiological characterization of ammonia-oxidizing archaea and bacteria from freshwater, Appl Environ Microbiol, 78, 5773, 10.1128/AEM.00432-12 · DOI
  18. Galloway, 2008, Transformation of the nitrogen cycle: recent trends, questions, and potential solutions, Science, 320, 889, 10.1126/science.1136674 · DOI · Paper page
  19. Gruber, 2008, An Earth-system perspective of the global nitrogen cycle, Nature, 451, 293, 10.1038/nature06592 · DOI
  20. Gubry-Rangin, 2011, Niche specialization of terrestrial archaeal ammonia oxidizers, Proc Natl Acad Sci USA, 108, 21206, 10.1073/pnas.1109000108 · DOI
  21. Herrmann, 2009, Effect of lake trophic status and rooted macrophytes on community composition and abundance of ammonia-oxidizing prokaryotes in freshwater sediments, Appl Environ Microbiol, 75, 3127, 10.1128/AEM.02806-08 · DOI
  22. Hu, 2013, pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealed by high-throughput pyrosequencing, J Soils Sediments, 13, 1439, 10.1007/s11368-013-0726-y · DOI
  23. Hyman, 1992, 14C2H2- and 14CO2-labeling studies of the de novo synthesis of polypeptides by Nitrosomonas europaea during recovery from acetylene and light inactivation of ammonia monooxygenase, J Biol Chem, 267, 1534, 10.1016/S0021-9258(18)45979-0 · DOI
  24. Jia, 2009, Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil, Environ Microbiol, 11, 1658, 10.1111/j.1462-2920.2009.01891.x · DOI
  25. Kalbitz, 2013, The carbon count of 2000 years of rice cultivation, Global Change Biol, 19, 1107, 10.1111/gcb.12080 · DOI
  26. Ke, 2013, Niche differentiation of ammonia oxidizers and nitrite oxidizers in rice paddy soil, Environ Microbiol, 15, 2275, 10.1111/1462-2920.12098 · DOI
  27. Kim, 2012, Cultivation of a highly enriched ammonia-oxidizing archaeon of thaumarchaeotal group I.1b from an agricultural soil, Environ Microbiol, 14, 1528, 10.1111/j.1462-2920.2012.02740.x · DOI
  28. Kimura, 2000, Soil Biochemistry, 35
  29. Klotz, 2008, Nitrifier genomics and evolution of the nitrogen cycle, FEMS Microbiol Lett, 278, 146, 10.1111/j.1574-6968.2007.00970.x · DOI
  30. Koops, 2006, The Prokaryotes, 778, 10.1007/0-387-30745-1_36 · DOI
  31. Könneke, 2005, Isolation of an autotrophic ammonia-oxidizing marine archaeon, Nature, 437, 543, 10.1038/nature03911 · DOI
  32. Könneke, 2014, Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation, Proc Natl Acad Sci USA, 111, 8239, 10.1073/pnas.1402028111 · DOI
  33. Lehtovirta-Morley, 2011, Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil, Proc Natl Acad Sci USA, 108, 15892, 10.1073/pnas.1107196108 · DOI
  34. Liesack, 2000, Microbiology of flooded rice paddies, FEMS Microbiol Rev, 24, 625, 10.1111/j.1574-6976.2000.tb00563.x · DOI
  35. Liew, 2014, Mutagenesis of the hydrocarbon monooxygenase indicates a metal centre in subunit-C, and not subunit-B, is essential for copper-containing membrane monooxygenase activity, Microbiology, 160, 1267, 10.1099/mic.0.078584-0 · DOI
  36. Lu, 2013, Urease gene-containing Archaea dominate autotrophic ammonia oxidation in two acid soils, Environ Microbiol, 15, 1795, 10.1111/1462-2920.12071 · DOI
  37. Lücker, 2010, A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria, Proc Natl Acad Sci USA, 107, 13479, 10.1073/pnas.1003860107 · DOI
  38. Martens-Habbena, 2009, Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria, Nature, 461, 976, 10.1038/nature08465 · DOI
  39. Morrill, 1962, Growth rates of nitrifying chemoautotrophs in soil, J Bacteriol, 83, 205, 10.1128/jb.83.1.205-206.1962 · DOI
  40. Off, 2010, Enrichment and physiological characterization of a novel Nitrospira-like bacterium obtained from a marine sponge, Appl Environ Microbiol, 76, 4640, 10.1128/AEM.00320-10 · DOI
  41. Pett-Ridge, 2013, Influence of oxic/anoxic fluctuations on ammonia oxidizers and nitrification potential in a wet tropical soil, FEMS Microbiol Ecol, 85, 179, 10.1111/1574-6941.12111 · DOI
  42. Prosser, 2012, Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation, Trends Microbiol, 20, 523, 10.1016/j.tim.2012.08.001 · DOI
  43. Rotthauwe, 1997, The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations, Appl Environ Microbiol, 63, 4704, 10.1128/aem.63.12.4704-4712.1997 · DOI
  44. Santoro, 2011, Isotopic signature of N2O produced by marine ammonia-oxidizing archaea, Science, 333, 1282, 10.1126/science.1208239 · DOI
  45. Schleper, 2010, Advances in Microbial Physiology, 1
  46. Schloss, 2009, Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities, Appl Environ Microbiol, 75, 7537, 10.1128/AEM.01541-09 · DOI
  47. Schramm, 2000, Microenvironments and distribution of nitrifying bacteria in a membrane-bound biofilm, Environ Microbiol, 2, 680, 10.1046/j.1462-2920.2000.00150.x · DOI
  48. Schramm, 1999, Microscale distribution of populations and activities of Nitrosospira and Nitrospira spp. along a macroscale gradient in a nitrifying bioreactor: quantification by in situ hybridization and the use of microsensors, Appl Environ Microbiol, 65, 3690, 10.1128/AEM.65.8.3690-3696.1999 · DOI
  49. Sebilo, 2013, Long-term fate of nitrate fertilizer in agricultural soils, Proc Natl Acad Sci USA, 110, 18185, 10.1073/pnas.1305372110 · DOI
  50. Sorokin, 2012, Nitrification expanded: discovery, physiology and genomics of a nitrite-oxidizing bacterium from the phylum Chloroflexi, ISME J, 6, 2245, 10.1038/ismej.2012.70 · DOI
  51. Stieglmeier, 2014, Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea, ISME J, 8, 1135, 10.1038/ismej.2013.220 · DOI
  52. Tamura, 2007, MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0, Mol Biol Evol, 24, 1596, 10.1093/molbev/msm092 · DOI
  53. Tourna, 2008, Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms, Environ Microbiol, 10, 1357, 10.1111/j.1462-2920.2007.01563.x · DOI
  54. Verhamme, 2011, Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms, ISME J, 5, 1067, 10.1038/ismej.2010.191 · DOI
  55. Walker, 2010, Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea, Proc Natl Acad Sci USA, 107, 8818, 10.1073/pnas.0913533107 · DOI
  56. Webster, 2005, Links between ammonia oxidizer species composition, functional diversity and nitrification kinetics in grassland soils, Environ Microbiol, 7, 676, 10.1111/j.1462-2920.2005.00740.x · DOI
  57. Xia, 2011, Autotrophic growth of nitrifying community in an agricultural soil, ISME J, 5, 1226, 10.1038/ismej.2011.5 · DOI
  58. Yan, 2003, Estimation of nitrous oxide, nitric oxide and ammonia emissions from croplands in East, Southeast and South Asia, Glob Change Biol, 9, 1080, 10.1046/j.1365-2486.2003.00649.x · DOI
  59. Zhang, 2009, Denitrification and total nitrogen gas production from forest soils of Eastern China, Soil Biol Biochem, 41, 2551, 10.1016/j.soilbio.2009.09.016 · DOI

Metadata

Authors
Wang, B., Zhao, J., Guo, Z., Ma, J., Xu, H., & Jia, Z.
Affiliations
Chinese Academy of Sciences (CN)
Corresponding author
Jia, Zhongjun
Venue
The ISME Journal
Published
2014-10-10
Volume
9
Issue
5
Pages
1062-1075
ISSN
  • 1751-7362 (ISSN-L)
  • 1751-7370
OpenAlex
W2054606614
Cited by
225
References
1
Citations by year
2026: 14 · 2025: 13 · 2024: 21 · 2023: 16 · 2022: 24 · 2021: 30 · 2020: 26 · 2019: 26 · 2018: 27 · 2017: 17 · 2016: 8 · 2015: 3
FWCI
12.27
Type
journal article
Language
en
Open access
Locations
  • The ISME Journal (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
Funders
  • National Natural Science Foundation of China (XDB15040000, 41101227, 41090281)
  • Chinese Academy of Sciences (XDB15040000)
  • Government of Jiangsu Province
Topics
  • Life Sciences › Agricultural and Biological Sciences › Soil Science › Soil Carbon and Nitrogen Dynamics
  • Physical Sciences › Environmental Science › Pollution › Wastewater Treatment and Nitrogen Removal
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords
nitrification, ammonia-oxidizing archaea, ammonia-oxidizing bacteria, nitrite-oxidizing bacteria, paddy soil, paddy fields, amoA gene, stable isotope probing, Nitrososphaera, Nitrosomonas, Nitrospira, Nitrobacter, nitrogen cycling
MeSH terms
Agriculture, Ammonia, Archaea, Bacteria, China, Nitrites, Nitrogen, Oxidation-Reduction, Phylogeny, Oryza, RNA, Ribosomal, 16S, Soil, Soil Microbiology, Ecosystem, Betaproteobacteria, Nitrification

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review