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Effects of Water-Saving Irrigation on Emissions of Greenhouse Gases and Prokaryotic Communities in Rice Paddy Soil

  • Environmental Microbiology
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Abstract

The effects of water-saving irrigation on emissions of greenhouse gases and soil prokaryotic communities were investigated in an experimental rice field. The water layer was kept at 1–2 cm in the water-saving (WS) irrigation treatment and at 6 cm in the continuous flooding (CF) irrigation treatment. WS irrigation decreased CH4 emissions by 78 % and increased N2O emissions by 533 %, resulting in 78 % reduction of global warming potential compared to the CF irrigation. WS irrigation did not affect the abundance or phylogenetic distribution of bacterial/archaeal 16S rRNA genes and the abundance of bacterial/archaeal 16S rRNAs. The transcript abundance of CH4 emission-related genes generally followed CH4 emission patterns, but the difference in abundance between mcrA transcripts and amoA/pmoA transcripts best described the differences in CH4 emissions between the two irrigation practices. WS irrigation increased the relative abundance of 16S rRNAs and functional gene transcripts associated with Anaeromyxobacter and Methylocystis spp., suggesting that their activities might be important in emissions of the greenhouse gases. The N2O emission patterns were not reflected in the abundance of N2O emission-related genes and transcripts. We showed that the alternative irrigation practice was effective for mitigating greenhouse gas emissions from rice fields and that it did not affect the overall size and structure of the soil prokaryotic community but did affect the activity of some groups.

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References

  1. IPCC (2007) IPCC fourth assessment report: climate change 2007 synthesis report. IPCC, Geneva

    Google Scholar 

  2. Linquist B, van Groenigen KJ, Adviento-Borbe MA, Pittelkow C, van Kessel C (2012) An agronomic assessment of greenhouse gas emissions from major cereal crops. Glob Chang Biol 18:194–209

    Article  Google Scholar 

  3. Yan X, Yagi K, Akiyama H, Akimoto H (2005) Statistical analysis of the major variables controlling methane emission from rice fields. Glob Chang Biol 11:1131–1141

    Article  Google Scholar 

  4. Linquist BA, Adviento-Borbe MA, Pittelkow CM, van Kessel C, van Groenigen KJ (2012) Fertilizer management practices and greenhouse gas emissions from rice systems: a quantitative review and analysis. Field Crop Res 135:10–21

    Article  Google Scholar 

  5. Yan X, Akiyama H, Yagi K, Akimoto H (2009) Global estimations of the inventory and mitigation potential of methane emissions from rice cultivation conducted using the 2006 Intergovernmental Panel on Climate Change Guidelines. Global Biogeochem Cy 23:GB2002

  6. Yang S, Peng S, Xu J, Luo Y, Li D (2012) Methane and nitrous oxide emissions from paddy field as affected by water-saving irrigation. Phys Chem Earth Pt A/B/C 53–54:30–37

    Article  Google Scholar 

  7. Suryavanshi P, Singh YV, Prasanna R, Bhatia A, Shivay YS (2013) Pattern of methane emission and water productivity under different methods of rice crop establishment. Paddy Water Environ 11:321–329

    Article  Google Scholar 

  8. Hou H, Peng S, Xu J, Yang S, Mao Z (2012) Seasonal variations of CH4 and N2O emissions in response to water management of paddy fields located in Southeast China. Chemosphere 89:884–892

    Article  CAS  PubMed  Google Scholar 

  9. Jiao Z, Hou A, Shi Y, Huang G, Wang Y et al (2006) Water management influencing methane and nitrous oxide emissions from rice field in relation to soil redox and microbial community. Commun Soil Sci Plant 37:1889–1903

    Article  CAS  Google Scholar 

  10. Cai Z-C, Xing G-X, Shen G-Y, Xu H, Yan X-Y et al (1999) Measurements of CH4 and N2O emissions from rice paddies in Fengqiu, China. Soil Sci Plant Nutr 45:1–13

    Article  CAS  Google Scholar 

  11. Berger S, Jang I, Seo J, Kang H, Gebauer G (2013) A record of N2O and CH4 emissions and underlying soil processes of Korean rice paddies as affected by different water management practices. Biogeochemistry 1–16

  12. Hou AX, Chen GX, Wang ZP, Cleemput OV, Patrick WH Jr (2000) Methane and nitrous oxide emissions from a rice field in relation to soil redox and microbiological processes. Soil Sci Soc Am J 64:2180–2186

    Article  CAS  Google Scholar 

  13. Krüger M, Frenzel P, Conrad R (2001) Microbial processes influencing methane emission from rice fields. Glob Chang Biol 7:49–63

    Article  Google Scholar 

  14. Achtnich C, Bak F, Conrad R (1995) Competition for electron donors among nitrate reducers, ferric iron reducers, sulfate reducers, and methanogens in anoxic paddy soil. Biol Fert Soils 19:65–72

    Article  CAS  Google Scholar 

  15. Ratering S, Conrad R (1998) Effects of short-term drainage and aeration on the production of methane in submerged rice soil. Glob Chang Biol 4:397–407

    Article  Google Scholar 

  16. Watanabe T, Hosen Y, Agbisit R, Llorca L, Katayanagi N et al (2013) Changes in community structure of methanogenic archaea brought about by water-saving practice in paddy field soil. Soil Biol Biochem 58:235–243

    Article  CAS  Google Scholar 

  17. Ma K, Lu Y (2011) Regulation of microbial methane production and oxidation by intermittent drainage in rice field soil. FEMS Microbiol Ecol 75:446–456

    Article  CAS  PubMed  Google Scholar 

  18. Ma K, Conrad R, Lu Y (2012) Responses of methanogen mcrA genes and their transcripts to an alternate dry/wet cycle of paddy field soil. Appl Environ Microbiol 78:445–454

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. IPCC (1997) Greenhouse gas emissions from agricultural soils. In: Houghton JT et al. JT (eds) Greenhouse gas inventory reference manual revised 1996 IPCC guidelines for national greenhouse gas inventories. IPCC/OECD/IES. UK Meteorological Office, Bracknell

  20. Tuyrin IV (1951) To a method of the analysis for comparative structure studying soil organic matter or humus//Proc. of soil science institute by V. V. Dokuchaev (Trudi Pochvennogo Instituta by V. V. Dokuchaev) 38a: 5–21

  21. NIAST (1988) Methods of soil chemical analysis. National Institute of Agricultural Science and Technology (NIAST), Rural Development Administration (RDA), Suwon, Korea

  22. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Quince C, Lanzen A, Davenport R, Turnbaugh P (2011) Removing noise from pyrosequenced amplicons. BMC Bioinforma 12:38

    Article  Google Scholar 

  24. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Cole JR, Wang Q, Cardenas E, Fish J, Chai B et al (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W et al (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Pruesse E, Peplies J, Glöckner FO (2012) SINA: accurate high throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–1829

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Hamady M, Lozupone C, Knight R (2009) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4:17–27

    Article  PubMed Central  PubMed  Google Scholar 

  29. Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26:1641–1650

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539

    Article  PubMed Central  PubMed  Google Scholar 

  31. Ludwig W, Strunk O, Westram R, Richter L, Meier H et al (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Ludwig W, Strunk O, Klugbauer S, Klugbauer N, Weizenegger M et al (1998) Bacterial phylogeny based on comparative sequence analysis (review). Electrophoresis 19:554–568

    Article  CAS  PubMed  Google Scholar 

  33. Letunic I, Bork P (2011) Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39:W475–W478

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Xu Y, Ma K, Huang S, Liu L, Lu Y (2012) Diel cycle of methanogen mcrA transcripts in rice rhizosphere. Environ Microbiol Rep 4:655–663

    CAS  PubMed  Google Scholar 

  35. Lueders T, Chin K-J, Conrad R, Friedrich M (2001) Molecular analyses of methyl-coenzyme M reductase α-subunit (mcrA) genes in rice field soil and enrichment cultures reveal the methanogenic phenotype of a novel archaeal lineage. Environ Microbiol 3:194–204

    Article  CAS  PubMed  Google Scholar 

  36. Conrad R, Klose M, Noll M, Kemnitz D, Bodelier PLE (2008) Soil type links microbial colonization of rice roots to methane emission. Glob Chang Biol 14:657–669

    Article  Google Scholar 

  37. Zhang G, Ji Y, Ma J, Xu H, Cai Z et al (2012) Intermittent irrigation changes production, oxidation, and emission of CH4 in paddy fields determined with stable carbon isotope technique. Soil Biol Biochem 52:108–116

    Article  CAS  Google Scholar 

  38. Jones CM, Graf DRH, Bru D, Philippot L, Hallin S (2013) The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink. ISME J 7:417–426

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Sanford RA, Wagner DD, Wu Q, Chee-Sanford JC, Thomas SH et al (2012) Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proc Natl Acad Sci U S A 109:19709–19714

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. Drury CF, Findlay WI, McKenney DJ (1992) Nitric oxide and nitrous oxide production from soil: water and oxygen effects. Soil Sci Soc Am J 56:766–770

    Article  CAS  Google Scholar 

  41. Richardson D, Felgate H, Watmough N, Thomson A, Baggs E (2009) Mitigating release of the potent greenhouse gas N2O from the nitrogen cycle—could enzymic regulation hold the key? Trends Biotechnol 27:388–397

    Article  CAS  PubMed  Google Scholar 

  42. Morley N, Baggs EM, Dörsch P, Bakken L (2008) Production of NO, N2O and N2 by extracted soil bacteria, regulation by NO2 and O2 concentrations. FEMS Microbiol Ecol 65:102–112

    Article  CAS  PubMed  Google Scholar 

  43. Hori T, Noll M, Igarashi Y, Friedrich MW, Conrad R (2007) Identification of acetate-assimilating microorganisms under methanogenic conditions in anoxic rice field soil by comparative stable isotope probing of RNA. Appl Environ Microbiol 73:101–109

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. Sanford RA, Cole JR, Tiedje JM (2002) Characterization and description of Anaeromyxobacter dehalogenans gen. nov., sp. nov., an aryl-halorespiring facultative anaerobic Myxobacterium. Appl Environ Microbiol 68:893–900

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. He Q, Sanford RA (2003) Characterization of Fe(III) reduction by chlororespiring Anaeromxyobacter dehalogenans. Appl Environ Microbiol 69:2712–2718

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Thomas SH, Wagner RD, Arakaki AK, Skolnick J, Kirby JR et al (2008) The mosaic genome of Anaeromyxobacter dehalogenans strain 2CP-C suggests an aerobic common ancestor to the Delta-Proteobacteria. PLoS ONE 3:e2103

    Article  PubMed Central  PubMed  Google Scholar 

  47. Stein LY, Yung YL (2003) Production, isotopic composition, and atmospheric fate of biologically produced nitrous oxide. Annu Rev Earth Pl Sc 31:329–356

    Article  CAS  Google Scholar 

  48. Mandernack KW, Kinney CA, Coleman D, Huang Y-S, Freeman KH et al (2000) The biogeochemical controls of N2O production and emission in landfill cover soils: the role of methanotrophs in the nitrogen cycle. Environ Microbiol 2:298–309

    Article  CAS  PubMed  Google Scholar 

  49. Mills HJ, Martinez RJ, Story S, Sobecky PA (2005) Characterization of microbial community structure in Gulf of Mexico gas hydrates: comparative analysis of DNA- and RNA-derived clone libraries. Appl Environ Microbiol 71:3235–3247

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  50. Martinez RJ, Mills HJ, Story S, Sobecky PA (2006) Prokaryotic diversity and metabolically active microbial populations in sediments from an active mud volcano in the Gulf of Mexico. Environ Microbiol 8:1783–1796

    Article  CAS  PubMed  Google Scholar 

  51. Lloyd KG, Lapham L, Teske A (2006) An anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline Gulf of Mexico sediments. Appl Environ Microbiol 72:7218–7230

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  52. Knittel K, Boetius A (2009) Anaerobic oxidation of methane: progress with an unknown process. Annu Rev Microbiol 63:311–334

    Article  CAS  PubMed  Google Scholar 

  53. Conrad R (2007) Microbial ecology of methanogens and methanotrophs. Adv Agron 96:1–63

    Article  CAS  Google Scholar 

  54. Miyashita A, Mochimaru H, Kazama H, Ohashi A, Yamaguchi T et al (2009) Development of 16S rRNA gene-targeted primers for detection of archaeal anaerobic methanotrophs (ANMEs). FEMS Microbiol Lett 297:31–37

    Article  CAS  PubMed  Google Scholar 

  55. Bédard C, Knowles R (1989) Physiology, biochemistry, and specific inhibitors of CH4, NH4 +, and CO oxidation by methanotrophs and nitrifiers. Microbiol Rev 53:68–84

    PubMed Central  PubMed  Google Scholar 

  56. Bodelier PLE, Frenzel P (1999) Contribution of methanotrophic and nitrifying bacteria to CH4 and NH4 + oxidation in the rhizosphere of rice plants as determined by new methods of discrimination. Appl Environ Microbiol 65:1826–1833

    PubMed Central  CAS  PubMed  Google Scholar 

  57. Klemedtsson L, Jiang Q, Kasimir Klemedtsson Å, Bakken L (1999) Autotrophic ammonium-oxidising bacteria in Swedish mor humus. Soil Biol Biochem 31:839–847

    Article  CAS  Google Scholar 

  58. Braker G, Conrad R (2011) Chapter 2—diversity, structure, and size of N2O-producing microbial communities in soils—what matters for their functioning? Adv Appl Microbiol 75:33–70

    Article  CAS  PubMed  Google Scholar 

  59. Hendriks J, Oubrie A, Castresana J, Urbani A, Gemeinhardt S et al (2000) Nitric oxide reductases in bacteria. BBA-Bioenergetics 1459:266–273

    Article  CAS  PubMed  Google Scholar 

  60. Casciotti KL, Ward BB (2005) Phylogenetic analysis of nitric oxide reductase gene homologues from aerobic ammonia-oxidizing bacteria. FEMS Microbiol Ecol 52:197–205

    Article  CAS  PubMed  Google Scholar 

  61. Stein LY, Klotz MG (2011) Nitrifying and denitrifying pathways of methanotrophic bacteria. Biochem Soc T 39:1826–1831

    Article  CAS  Google Scholar 

  62. García-Lledó A, Vilar-Sanz A, Trias R, Hallin S, Bañeras L (2011) Genetic potential for N2O emissions from the sediment of a free water surface constructed wetland. Water Res 45:5621–5632

    Article  PubMed  Google Scholar 

  63. Philippot L, Andert J, Jones CM, Bru D, Hallin S (2011) Importance of denitrifiers lacking the genes encoding the nitrous oxide reductase for N2O emissions from soil. Glob Chang Biol 17:1497–1504

    Article  Google Scholar 

  64. Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM et al (2009) Three genomes from the phylum Acidobacteria provide insight into the life styles of these microorganisms in soils. Appl Environ Microbiol 75:2046–2056

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  65. Belasco JG, Biggins CF (1988) Mechanisms of mRNA decay in bacteria: a perspective. Gene 72:15–23

    Article  CAS  PubMed  Google Scholar 

  66. Higgins CF (1991) Stability and degradation of mRNA. Curr Opin Cell Biol 3:1013–1018

    Article  CAS  PubMed  Google Scholar 

  67. Hierro N, Esteve-Zarzoso B, González Á, Mas A, Guillamón JM (2006) Real-time quantitative PCR (QPCR) and reverse transcription-QPCR for detection and enumeration of total yeasts in wine. Appl Environ Microbiol 72:7148–7155

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  68. Gilbert B, Frenzel P (1998) Rice roots and CH4 oxidation: the activity of bacteria, their distribution and the microenvironment. Soil Biol Biochem 30:1903–1916

    Article  CAS  Google Scholar 

  69. Philippot L, Hallin S, Börjesson G, Baggs EM (2009) Biochemical cycling in the rhizosphere having an impact on global change. Plant Soil 321:61–81

    Article  CAS  Google Scholar 

  70. Ma K, Conrad R, Lu Y (2013) Dry/wet cycles change the activity and population dynamics of methanotrophs in rice field soil. Appl Environ Microbiol 79:4932–4939

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  71. Arth I, Frenzel P, Conrad R (1998) Denitrification coupled to nitrification in the rhizosphere of rice. Soil Biol Biochem 30:509–515

    Article  CAS  Google Scholar 

  72. Arth I, Frenzel P (2000) Nitrification and denitrification in the rhizosphere of rice: the detection of processes by a new multi-channel electrode. Biol Fertil Soils 31:427–435

    Article  CAS  Google Scholar 

  73. Wertz S, Dandie CE, Goyer C, Trevors JT, Patten CL (2009) Diversity of nirK denitrifying genes and transcripts in an agricultural soil. Appl Environ Microbiol 75:7365–7377

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  74. Yoshida M, Ishii S, Fujii D, Otsuka S, Senoo K (2012) Identification of active denitrifiers in rice paddy soil by DNA- and RNA-based analyses. Microbes Environ 27:456–461

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgement

This study was carried out with the support of “Research Program for Agricultural Science and Technology Development (Project No. PJ010036)”, National Academy of Agricultural Science, Rural Development Administration, Republic of Korea.

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Correspondence to Gun-Yeob Kim or Hang-Yeon Weon.

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Ahn, JH., Choi, MY., Kim, BY. et al. Effects of Water-Saving Irrigation on Emissions of Greenhouse Gases and Prokaryotic Communities in Rice Paddy Soil. Microb Ecol 68, 271–283 (2014). https://doi.org/10.1007/s00248-014-0371-z

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