Journal of Soils and Sediments

, Volume 19, Issue 1, pp 23–37 | Cite as

Distributions and environmental drivers of archaea and bacteria in paddy soils

  • Chao-Lei Yuan
  • Li-Mei Zhang
  • Jun-Tao Wang
  • Hang-Wei Hu
  • Ju-Pei Shen
  • Peng Cao
  • Ji-Zheng HeEmail author
Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article



The aim of this study is to investigate the abundance, diversity, and distribution of archaea and bacteria as affected by environment parameters in paddy soils, with focus on putative functional microbial groups related to redox processes. Because there is generally a high iron content in the soil, we also want to test a hypothesis that soil iron concentration significantly affects microbial diversity and distribution.

Materials and methods

Quantitative PCR and barcoded pyrosequencing of 16S ribosomal RNA genes were employed to investigate the abundance and community composition of archaeal and bacterial communities in 27 surface paddy soil samples. Pearson’s correlation, analysis of variance, partial least squares regression, principal coordinates analysis, and structural equation models were performed for the analyses of gene copy numbers, α-diversity, β-diversity, and relative abundances of archaea and bacteria and their relationships with environmental factors.

Results and discussion

Archaeal abundance was correlated greatest with temperature, but bacterial abundance was affected mainly by soil organic matter and total nitrogen content. Soil pH and concentrations of different ions were associated with archaeal and bacterial β-diversity. The relative abundances of Euryarchaeota and Thaumarchaeota were 61.3 and 13.1% of archaea and correlated with soil pH, which may affect the availability of substrates to methanogens and ammonia oxidizers. Dominant bacterial phyla were Proteobacteria (32.4%), Acidobacteria (17.8%), Bacteroidetes (9.3%), and Verrucomicrobia (6.0%). The relative abundances of putative bacterial reducers of nitrate, Fe(III), sulfate, and sulfur, and oxidizers of ammonia, nitrite, reduced sulfur, and C1 compounds had positive, negative, or non-significant correlations with the concentrations of their substrates. Soil iron concentration was correlated only with the distributions of some putative iron-reducing bacteria.


In paddy soils characterized by dynamic redox processes, archaea and bacteria differ in relationships of abundance, diversity, and distribution with environmental factors. Especially, the concentrations of electron donors or acceptors can explain the distributions of some but not all the putative functional microbial groups related to redox processes. Depending on pH range, soil pH has a strong impact on microbial ecology in paddy soils.


Archaea Bacteria Distribution Putative functional groups Paddy soil 


Funding information

This work was financially supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15020201), the National Natural Science Foundation of China (41601239), the China Postdoctoral Science Foundation (2016M600644), the “Pearl River Talents” Postdoctoral Program of Guangdong Province, the National Key Research and Development Program of China (2016YFD0800703), and the High-level Leading Talent Introduction Program of GDAS.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11368_2018_1997_MOESM1_ESM.docx (2.2 mb)
ESM 1 (DOCX 2.24 mb)


  1. Barns SM, Cain EC, Sommerville L, Kuske CR (2007) Acidobacteria phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Appl Environ Microbiol 73:3113–3116CrossRefGoogle Scholar
  2. Barton NH, Briggs DEG, Eisen JA, Goldstein DB, Patel NH (2007) Evolution. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  3. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252CrossRefGoogle Scholar
  4. Canfield DE, Thamdrup B, Hansen JW (1993) The anaerobic degradation of organic matter in Danish coastal sediments: iron reduction, manganese reduction, and sulfate reduction. Geochim Cosmochim Acta 57:3867–3883CrossRefGoogle Scholar
  5. Cao P, Zhang LM, Shen JP, Zheng YM, Di HJ, He JZ (2012) Distribution and diversity of archaeal communities in selected Chinese soils. FEMS Microbiol Ecol 80:146–158CrossRefGoogle Scholar
  6. Carlson HK, Clark IC, Blazewicz SJ, Iavarone AT, Coates JD (2013) Fe(II) oxidation is an innate capability of nitrate-reducing bacteria that involves abiotic and biotic reactions. J Bacteriol 195:3260–3268CrossRefGoogle Scholar
  7. Carson JK, Gonzalez-Quinones V, Murphy DV, Hinz C, Shaw JA, Gleeson DB (2010) Low pore connectivity increases bacterial diversity in soil. Appl Environ Microbiol 76:3936–3942CrossRefGoogle Scholar
  8. Chapin FS, Matson PA, Mooney HA (2002) Principles of terrestrial ecosystem ecology. Springer, New YorkGoogle Scholar
  9. Chau JF, Bagtzoglou AC, Willig MR (2011) The effect of soil texture on richness and diversity of bacterial communities. Environ Forensic 12:333–341CrossRefGoogle Scholar
  10. Chen XP, Zhu YG, Xia Y, Shen JP, He JZ (2008) Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? Environ Microbiol 10:1978–1987CrossRefGoogle Scholar
  11. Chistoserdova L, Lidstrom ME (2013) Aerobic methylotrophic prokaryotes. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: prokaryotic physiology and biochemistry. Springer, Berlin, pp 267–285CrossRefGoogle Scholar
  12. Chu HY, Fierer N, Lauber CL, Caporaso JG, Knight R, Grogan P (2010) Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ Microbiol 12:2998–3006CrossRefGoogle Scholar
  13. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145CrossRefGoogle Scholar
  14. Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard RH, von Bergen M, Rattei T, Bendinger B, Nielsen PH, Wagner M (2015) Complete nitrification by Nitrospira bacteria. Nature 528:504–509CrossRefGoogle Scholar
  15. Daims H, Lucker S, Wagner M (2016) A new perspective on microbes formerly known as nitrite-oxidizing bacteria. Trends Microbiol 24:699–712CrossRefGoogle Scholar
  16. Delgado-Baquerizo M, Bissett A, Eldridge DJ, Maestre FT, He J-Z, Wang J-T, Hamonts K, Liu Y-R, Singh BK, Fierer N (2017) Palaeoclimate explains a unique proportion of the global variation in soil bacterial communities. Nature Ecol Evol 1:1339–1347CrossRefGoogle Scholar
  17. Ding L-J, Su J-Q, Xu H-J, Jia Z-J, Zhu Y-G (2015) Long-term nitrogen fertilization of paddy soil shifts iron-reducing microbial community revealed by RNA-13C-acetate probing coupled with pyrosequencing. ISME J 9:721–734CrossRefGoogle Scholar
  18. Eller G, Krüger M, Frenzel P (2005) Comparing field and microcosm experiments: a case study on methano- and methylo-trophic bacteria in paddy soil. FEMS Microbiol Ecol 51:279–291CrossRefGoogle Scholar
  19. Emerson D, Fleming EJ, McBeth JM (2010) Iron-oxidizing bacteria: an environmental and genomic perspective. Annu Rev Microbiol 64:561–583CrossRefGoogle Scholar
  20. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631CrossRefGoogle Scholar
  21. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364CrossRefGoogle Scholar
  22. Garcia J-L, Patel BKC, Ollivier B (2000) Taxonomic, phylogenetic, and ecological diversity of methanogenic archaea. Anaerobe 6:205–226CrossRefGoogle Scholar
  23. Griffiths RI, Thomson BC, James P, Bell T, Bailey M, Whiteley AS (2011) The bacterial biogeography of British soils. Environ Microbiol 13:1642–1654CrossRefGoogle Scholar
  24. Gubry-Rangin C, Hai B, Quince C, Engel M, Thomson BC, James P, Schloter M, Griffiths RI, Prosser JI, Nicol GW (2011) Niche specialization of terrestrial archaeal ammonia oxidizers. Proc Natl Acad Sci U S A 108:21206–21211CrossRefGoogle Scholar
  25. Haveman SA, Greene EA, Stilwell CP, Voordouw JK, Voordouw G (2004) Physiological and gene expression analysis of inhibition of Desulfovibrio vulgaris Hildenborough by nitrite. J Bacteriol 186:7944–7950CrossRefGoogle Scholar
  26. He JZ, Hu HW, Zhang LM (2012) Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils. Soil Biol Biochem 55:146–154CrossRefGoogle Scholar
  27. Hu H-W, He J-Z (2017) Comammox—a newly discovered nitrification process in the terrestrial nitrogen cycle. J Soils Sediments 17:2709–2717CrossRefGoogle Scholar
  28. Hu H-W, Zhang L-M, Dai Y, Di H-J, He J-Z (2013a) pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealed by high-throughput pyrosequencing. J Soils Sediments 13:1439–1449CrossRefGoogle Scholar
  29. Hu H-W, Zhang L-M, Yuan C-L, He J-Z (2013b) Contrasting Euryarchaeota communities between upland and paddy soils exhibited similar pH-impacted biogeographic patterns. Soil Biol Biochem 64:18–27CrossRefGoogle Scholar
  30. Hu H-W, Zhang L-M, Yuan C-L, Zheng Y, Wang J-T, Chen D, He J-Z (2015) The large-scale distribution of ammonia oxidizers in paddy soils is driven by soil pH, geographic distance, and climatic factors. Frontier Microbiol 6:938Google Scholar
  31. Hubert C, Voordouw G (2007) Oil field souring control by nitrate-reducing Sulfurospirillum spp. that outcompete sulfate-reducing bacteria for organic electron donors. Appl Environ Microbiol 73:2644–2652CrossRefGoogle Scholar
  32. Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:1889–1898CrossRefGoogle Scholar
  33. Hussain Q, Liu Y, Zhang A, Pan G, Li L, Zhang X, Song X, Cui L, Jin Z (2011) Variation of bacterial and fungal community structures in the rhizosphere of hybrid and standard rice cultivars and linkage to CO2 flux. FEMS Microbiol Ecol 78:116–128CrossRefGoogle Scholar
  34. Ishii S, Yamamoto M, Kikuchi M, Oshima K, Hattori M, Otsuka S, Senoo K (2009) Microbial populations responsive to denitrification-inducing conditions in rice paddy soil, as revealed by comparative 16S rRNA gene analysis. Appl Environ Microbiol 75:7070–7078CrossRefGoogle Scholar
  35. Jiang Y, Liang Y, Li C, Wang F, Sui Y, Suvannang N, Zhou J, Sun B (2016) Crop rotations alter bacterial and fungal diversity in paddy soils across East Asia. Soil Biol Biochem 95:250–261CrossRefGoogle Scholar
  36. Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453CrossRefGoogle Scholar
  37. Kaster K, Grigoriyan A, Jennneman G, Voordouw G (2007) Effect of nitrate and nitrite on sulfide production by two thermophilic, sulfate-reducing enrichments from an oil field in the North Sea. Appl Microbiol Biotechnol 75:195–203CrossRefGoogle Scholar
  38. Ke X, Angel R, Lu Y, Conrad R (2013) Niche differentiation of ammonia oxidizers and nitrite oxidizers in rice paddy soil. Environ Microbiol 15:2275–2292CrossRefGoogle Scholar
  39. Kelly DP, Wood AP, Stackebrandt E (2015) Thiobacillus, Bergey’s manual of systematics of archaea and bacteria. John Wiley & Sons, Ltd, LondonGoogle Scholar
  40. Kemnitz D, Kolb S, Conrad R (2005) Phenotypic characterization of rice cluster III archaea without prior isolation by applying quantitative polymerase chain reaction to an enrichment culture. Environ Microbiol 7:553–565CrossRefGoogle Scholar
  41. Kettler TA, Doran JW, Gilbert TL (2001) Simplified method for soil particle-size determination to accompany soil-quality analyses. Soil Sci Soc Am J 65:849–852CrossRefGoogle Scholar
  42. Kirk G (2004) The biogeochemistry of submerged soils. John Wiley & Sons, LondonCrossRefGoogle Scholar
  43. Kögel-Knabner I, Amelung W, Cao Z, Fiedler S, Frenzel P, Jahn R, Kalbitz K, Kölbl A, Schloter M (2010) Biogeochemistry of paddy soils. Geoderma 157:1–14CrossRefGoogle Scholar
  44. Koops H-P, Pommerening-Röser A (2015) The lithoautotrophic ammonia-oxidizing bacteria. In: Bergey’s manual of systematics of archaea and bacteria. John Wiley & Sons, Ltd.
  45. Kuever J, Rainey FA, Widdel F (2015) Desulfuromonas, Bergey’s manual of systematics of archaea and bacteria. John Wiley & Sons, Ltd, HobokenGoogle Scholar
  46. Lane D (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, p 133Google Scholar
  47. Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120CrossRefGoogle Scholar
  48. Li Y, Yu S, Strong J, Wang H (2012) Are the biogeochemical cycles of carbon, nitrogen, sulfur, and phosphorus driven by the “FeIII–FeII redox wheel” in dynamic redox environments? J Soils Sediments 12:683–693CrossRefGoogle Scholar
  49. Li X, Zhang W, Liu T, Chen L, Chen P, Li F (2016) Changes in the composition and diversity of microbial communities during anaerobic nitrate reduction and Fe(II) oxidation at circumneutral pH in paddy soil. Soil Biol Biochem 94:70–79CrossRefGoogle Scholar
  50. Liesack W, Finster K (2015) Desulfuromusa. In: Bergey’s manual of systematics of archaea and bacteria. John Wiley & Sons, Ltd.
  51. Liesack W, Schnell S, Revsbech N (2000) Microbiology of flooded rice paddies. FEMS Microbiol Rev 24:625–645CrossRefGoogle Scholar
  52. Liu X-Z, Zhang L-M, Prosser JI, He J-Z (2009) Abundance and community structure of sulfate reducing prokaryotes in a paddy soil of southern China under different fertilization regimes. Soil Biol Biochem 41:687–694CrossRefGoogle Scholar
  53. Loeppert RH, Inskeep WP (1996) Iron. In: Sparks DL, Page AL, Helmke PA, Loeppert RH (eds) Methods of soil analysis Part 3—Chemical methods, SSSA Book Series. Soil Science Society of America, American Society of Agronomy, Madison, pp 639–664Google Scholar
  54. Lovley D (2013) Dissimilatory Fe(III)- and Mn(IV)-reducing prokaryotes. In: Rosenberg E, DeLong E, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes. Springer, Berlin, pp 287–308CrossRefGoogle Scholar
  55. Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn(IV) reduction, advances in microbial physiology. Academic Press, Cambridge, pp 219–286Google Scholar
  56. Ma K, Qiu QF, Lu YH (2010) Microbial mechanism for rice variety control on methane emission from rice field soil. Glob Chang Biol 16:3085–3095CrossRefGoogle Scholar
  57. Ma B, Dai Z, Wang H, Dsouza M, Liu X, He Y, Wu J, Rodrigues JLM, Gilbert JA, Brookes PC, Xu J (2017) Distinct biogeographic patterns for archaea, bacteria, and fungi along the vegetation gradient at the continental scale in Eastern China. mSystems 2:e00174-16CrossRefGoogle Scholar
  58. Maestre FT, Delgado-Baquerizo M, Jeffries TC, Eldridge DJ, Ochoa V, Gozalo B, Quero JL, García-Gómez M, Gallardo A, Ulrich W, Bowker MA, Arredondo T, Barraza-Zepeda C, Bran D, Florentino A, Gaitán J, Gutiérrez JR, Huber-Sannwald E, Jankju M, Mau RL, Miriti M, Naseri K, Ospina A, Stavi I, Wang D, Woods NN, Yuan X, Zaady E, Singh BK (2015) Increasing aridity reduces soil microbial diversity and abundance in global drylands. Proc Natl Acad Sci U S A 112:15684–15689Google Scholar
  59. McDonald JH (2014) Handbook of biological statistics. Sparky House, BaltimoreGoogle Scholar
  60. Muyzer G, Kuenen JG, Robertson LA (2013) Colorless sulfur Bacteria. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: prokaryotic physiology and biochemistry. Springer, Berlin, pp 555–588CrossRefGoogle Scholar
  61. Myers CR, Nealson KH (1988) Microbial reduction of manganese oxides: interactions with iron and sulfur. Geochim Cosmochim Acta 52:2727–2732CrossRefGoogle Scholar
  62. Neculita C-M, Zagury GJ, Bussiere B (2007) Passive treatment of acid mine drainage in bioreactors using sulfate-reducing bacteria: critical review and research needs. J Environ Qual 36(1):16CrossRefGoogle Scholar
  63. Ponnamperuma F (1972) The chemistry of submerged soils. Adv Agron 24:29CrossRefGoogle Scholar
  64. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig WG, Peplies J, Glockner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196CrossRefGoogle Scholar
  65. Rabus R, Hansen TA, Widdel F (2013) Dissimilatory sulfate- and sulfur-reducing prokaryotes. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: prokaryotic physiology and biochemistry. Springer, Berlin, pp 309–404CrossRefGoogle Scholar
  66. Ratering S, Schnell S (2001) Nitrate-dependent iron(II) oxidation in paddy soil. Environ Microbiol 3:100–109CrossRefGoogle Scholar
  67. Schink B (2015) Pelobacter, Bergey’s manual of systematics of archaea and bacteria. John Wiley & Sons, Ltd, HobokenGoogle Scholar
  68. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefGoogle Scholar
  69. Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:e27310CrossRefGoogle Scholar
  70. Shapleigh JP (2013) Denitrifying Prokaryotes. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: prokaryotic physiology and biochemistry. Springer, Berlin, pp 405–425CrossRefGoogle Scholar
  71. Siles JA, Margesin R (2016) Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: what are the driving factors? Microb Ecol 72:207–220CrossRefGoogle Scholar
  72. Spieck E, Bock E (2015a) Nitrifying Bacteria. In: Bergey’s manual of systematics of archaea and Bacteria. John Wiley & Sons, Ltd, HobokenGoogle Scholar
  73. Spieck E, Bock E (2015b) The lithoautotrophic nitrite-oxidizing bacteria. In: Bergey’s manual of systematics of archaea and bacteria. John Wiley & Sons, Ltd, HobokenGoogle Scholar
  74. Stubner S, Wind T, Conrad R (1998) Sulfur oxidation in rice field soil: activity, enumeration, isolation and characterization of thiosulfate-oxidizing bacteria. Syst Appl Microbiol 21:569–578CrossRefGoogle Scholar
  75. Sun M, Xiao T, Ning Z, Xiao E, Sun W (2015) Microbial community analysis in rice paddy soils irrigated by acid mine drainage contaminated water. Appl Microbiol Biotechnol 99:2911–2922CrossRefGoogle Scholar
  76. Suzuki MT, Taylor LT, DeLong EF (2000) Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5′-nuclease assays. Appl Environ Microbiol 66:4605–4614CrossRefGoogle Scholar
  77. Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. John Wiley and Sons, Inc., New York, pp 179–244Google Scholar
  78. Valentine DL (2007) Adaptations to energy stress dictate the ecology and evolution of the archaea. Nat Rev Microbiol 5:316–323CrossRefGoogle Scholar
  79. van Kessel MAHJ, Speth DR, Albertsen M, Nielsen PH, Op den Camp HJM, Kartal B, Jetten MSM, Lücker S (2015) Complete nitrification by a single microorganism. Nature 528:555–559CrossRefGoogle Scholar
  80. Walkley A (1947) A critical examination of a rapid method for determining organic carbon in soils-effect of variations in digestion conditions and of inorganic soil constituents. Soil Sci 63:251–264CrossRefGoogle Scholar
  81. Wang B, Zhao J, Guo Z, Ma J, Xu H, Jia Z (2015) Differential contributions of ammonia oxidizers and nitrite oxidizers to nitrification in four paddy soils. ISME J 9:1062–1075CrossRefGoogle Scholar
  82. Wang JT, Zheng YM, Hu HW, Li J, Zhang LM, Chen BD, Chen WP, He JZ (2016) Coupling of soil prokaryotic diversity and plant diversity across latitudinal forest ecosystems. Sci Rep 6:19561CrossRefGoogle Scholar
  83. Witt C, Haefele SM (2005) Paddy soils. In: Daniel H (ed) Encyclopedia of soils in the environment. Elsevier, Oxford, pp 141–150CrossRefGoogle Scholar
  84. Wu MN, Qin HL, Chen Z, Wu JS, Wei WX (2011) Effect of long-term fertilization on bacterial composition in rice paddy soil. Biol Fertil Soils 47:397–405CrossRefGoogle Scholar
  85. Yuan YL, Conrad R, Lu YH (2009) Responses of methanogenic archaeal community to oxygen exposure in rice field soil. Environ Microbiol Rep 1:347–354CrossRefGoogle Scholar
  86. Yuan C, Fitzpatrick R, Mosley LM, Marschner P (2015a) Sulfate reduction in sulfuric material after re-flooding: effectiveness of organic carbon addition and pH increase depends on soil properties. J Hazard Mater 298:138–145CrossRefGoogle Scholar
  87. Yuan C, Mosley LM, Fitzpatrick R, Marschner P (2015b) Amount of organic matter required to induce sulfate reduction in sulfuric material after re-flooding is affected by soil nitrate concentration. J Environ Manag 151:437–442CrossRefGoogle Scholar
  88. Yuan C, Zhang L, Hu H, Wang J, Shen J, He J (2018) The biogeography of fungal communities in paddy soils is mainly driven by geographic distance. J Soils Sediments.
  89. Zhang W, Ding Y, Wang L, Rui W (2007) The significance of paddy ecosystems in environmental health and sustainable development of economy in the regions around Tai Lake. Sci Technol Rev 25:24–29 (in Chinese)Google Scholar
  90. Zhang L, Keller J, Yuan Z (2009) Inhibition of sulfate-reducing and methanogenic activities of anaerobic sewer biofilms by ferric iron dosing. Water Res 43:4123–4132CrossRefGoogle Scholar
  91. Zhang LM, Hu HW, Shen JP, He JZ (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6:1032–1045CrossRefGoogle Scholar
  92. Zhou J, Deng Y, Shen L, Wen C, Yan Q, Ning D, Qin Y, Xue K, Wu L, He Z, Voordeckers JW, Nostrand JDV, Buzzard V, Michaletz ST, Enquist BJ, Weiser MD, Kaspari M, Waide R, Yang Y, Brown JH (2016) Temperature mediates continental-scale diversity of microbes in forest soils. Nat Commun 7:12083CrossRefGoogle Scholar
  93. Zinger L, Lejon DPH, Baptist F, Bouasria A, Aubert S, Geremia RA, Choler P (2011) Contrasting diversity patterns of crenarchaeal, bacterial and fungal soil communities in an alpine landscape. PLoS One 6:e19950CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental SciencesChinese Academy of SciencesBeijingChina
  2. 2.Guangdong Key Laboratory of Integrated Agro-environmental Pollution Control and ManagementGuangdong Institute of Eco-environmental Science and TechnologyGuangzhouChina
  3. 3.Faculty of Veterinary and Agricultural SciencesThe University of MelbourneParkvilleAustralia

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