Impacts of waterlogging on soil nitrification and ammonia-oxidizing communities in farming system

  • Linh T. T. Nguyen
  • Yui Osanai
  • Ian C. Anderson
  • Michael P. Bange
  • Michael Braunack
  • David T. Tissue
  • Brajesh K. Singh
Regular Article

Abstract

Background and aims

Waterlogging may affect soil nitrification rates, resulting in changes in plant-available nitrogen (N), and hence potentially influencing crop productivity. Because nitrification is a microbially-driven process and ammonia-oxidizing communities regulate soil nitrification rates, the aim of this study was to investigate the mechanistic response of ammonia-oxidizing communities and nitrification rates to waterlogging.

Methods

A field study was conducted by experimentally imposing two short-term waterlogging events when cotton plants were at the early- and late-flowering stages. Soil physicochemical properties, nitrification rates, and ammonia-oxidizing community abundance and structure in response to waterlogging were examined.

Results

Soil nitrate (NO3) content, potential nitrification rates (PNR) and the abundance of ammonia-oxidizing communities significantly decreased upon waterlogging. Shifts in ammonia-oxidizing community structure were also observed. Both ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA) responded to waterlogging. PNR was significantly correlated with the abundance and structure of both AOB and AOA.

Conclusions

Waterlogging had strong negative effects on soil nitrification rates by altering the ammonia-oxidizing community abundance and structure, resulting in reduced soil N availability. Decreased plant-available N is likely to negatively affect primary productivity.

Keywords

Waterlogging Farming systems Nitrification Ammonia oxidiser communities 

Notes

Acknowledgments

We thank Dr. Hangwei Hu at the University of Melbourne, for providing supportive materials for TRFLP analysis. We acknowledge Dr. Jasmine Grinyer for her help in laboratory and comments on the manuscript and Dr. Collin Ahrens for providing statistical assistance. This work was financially supported by Hawkesbury Institute for the Environment and Western Sydney University. The work was carried out as a part of Cotton Research and Development Corporation project (UWS1301). BKS work is also supported Australian Research Council (DP170104634).

Supplementary material

11104_2018_3584_MOESM1_ESM.docx (426 kb)
ESM 1 (DOCX 425 kb)

References

  1. Bange M, Milroy S, Thongbai P (2004) Growth and yield of cotton in response to waterlogging. Field Crop Res 88:129–142CrossRefGoogle Scholar
  2. Bange MP, Baker J, Bauer P, Broughton KJ, Constable G, Luo Q, Osanai Y, Payton P, Tissue DT, Reddy K, Singh BK (2016) Climate change and cotton production in modern farming system. CABI Publication. Book, BostonCrossRefGoogle Scholar
  3. Barnard R, Leadley PW, Hungate BA (2005) Global change, nitrification, and denitrification: a review. Glob Biogeochem Cycles 19:GB1007.  https://doi.org/10.1029/2004GB002282 CrossRefGoogle Scholar
  4. Bates DM, Maechler M, Bolker B (2012) lme4: linear mixed-effects models using Eigen and S4. R Package Version 1.1–7. Available online at: http://CRAN.R-project.org/package=lme4
  5. Belser LW (1979) Population ecology of nitrifying bacteria. Annu Rev Microbiol 33:309–333CrossRefPubMedGoogle Scholar
  6. Bernhard A (2012) The nitrogen cycle: processes, players, and human impacts. Nature Education Knowledge 3(10):25Google Scholar
  7. Braunack M (2013) Cotton farming systems in Australia: factors contributing to changed yield and fibre quality. Crop Pasture Sci 64:834–844Google Scholar
  8. Chen Y, Xu Z, Hu H, Hu Y, Hao Z, Ziang Y, Chen B (2013) Responses of ammonia-oxidizing bacteria and archaea to nitrogen fertilization and precipitation increment in a typical temperate steppe in Inner Mongolia. Appl Soil Ecol 68:36–45CrossRefGoogle Scholar
  9. CRC (2010–2011) Cotton catchment communities CRC. Annual report “Cotton CRC campaign assists flooded cotton communities”Google Scholar
  10. Culman SW, Bukowski R, Gauch HG, Cadillo-quiroz H, Buckley DH (2009) T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinforms 10:171CrossRefGoogle Scholar
  11. Di H, Cameron K, Shen JP, Winefield C, O’Callaghan M, Bowatte S, He JZ (2009) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2:621–624CrossRefGoogle Scholar
  12. Di HJ, Cameron KC, Shen JP, Winefield CS, O'callaghan M, Bowatte S, He JZ (2010) Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol Ecol 72:386–394Google Scholar
  13. Engelaar WMHG, Bodelier PLE, Laanbroek HJ, Blom CWPM (1991) Nitrification in the rhizosphere of a flooding-resistant and a flooding-non-resistant Rumex species under drained and waterlogged conditions. FEMS Microbiol Ecol 86:33–42CrossRefGoogle Scholar
  14. Engelaar W, Symens J, Lannbroek H, Blom C (1995) Preservation of nitrifying capacity and nitrate availability in waterlogged soils by radial oxygen loss from roots of wetland plants. Biol Fertil Soils 20:243–248CrossRefGoogle Scholar
  15. Engelaar WM, Mastumaru T, Yoneyama T (2000) Combined effects of soil waterlogging and compaction on rice (Oryza Sativa L.) growth, soil aeration, soil N transformations and 15N discrimination. Biol Fertil Soils 32:484–493CrossRefGoogle Scholar
  16. Gieseke A, Tarre S, Green M, De Beer D (2006) Nitrification in a biofilm at low pH values: role of in situ microenvironments and acid tolerance. Appl Environ Microbiol 72:4283–4292CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gleeson DB, Müller C, Banerjee S, Ma W, Siciliano SD, Murphy DV (2010) Response of ammonia oxidizing archaea and bacteria to changing water filled pore space. Soil Biol Biochem 42:1888–1891CrossRefGoogle Scholar
  18. Greenway H, Armstrong W, Colmer TD (2006) Conditions leading to high CO2 (>5 kPa) in waterlogged–flooded soils and possible effects on root growth and metabolism. Ann Bot 98:9–32CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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 108:21206–21211CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hai B, Diallo NH, Sall S, Haesler F, Schauss K, Bonzi M, Assigbetse K, Chotte JL, Munch JC, Schloter M (2009) Quantification of key genes steering the microbial nitrogen cycle in the rhizosphere of sorghum cultivars in tropical agroecosystems. Appl Environ Microbiol 75:4993–5000CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hallin S, Jones CM, Schloter M, Philippot L (2009) Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3:597–605CrossRefPubMedGoogle Scholar
  22. Head L, Adams M, McGregor HV, Toole S (2014) Climate change and Australia. WIREs, Climate Change 5:175–197CrossRefGoogle Scholar
  23. Hirsch PR, Mauchline TH (2005) Chapter two – the importance of the microbial N cycle in soil for crop plant nutrition. Adv Appl Microbiol 93:45–71CrossRefGoogle Scholar
  24. Hodgson A, Chan K (1982) The effect of short-term waterlogging during furrow irrigation of cotton in a cracking grey clay. Crop Pasture Sci 33:109–116CrossRefGoogle Scholar
  25. Hu HW, Zhang LM, Dai Y, Di HJ, He JZ (2013) 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
  26. Hu HW, Macdonald CA, Trivedi P, Holmes B, Bodrossy L, He JZ, Singh BK (2015) Water addition regulates the metabolic activity of ammonia oxidizers responding to environmental perturbations in dry subhumid ecosystems. Environ Microbiol 17:444–461CrossRefPubMedGoogle Scholar
  27. Jackson MB, Drew MC (1984) Effects of flooding on growth and metabolism of herbaceous plants. Flooding Plant Growth 1:47–128CrossRefGoogle Scholar
  28. Kandeler E, Böhm KE (1996) Temporal dynamics of microbial biomass, xylanase activity, N-mineralisation and potential nitrification in different tillage systems. Appl Soil Ecol 4:181–191CrossRefGoogle Scholar
  29. Keeney D, Nelson D (1982) Nitrogen - inorganic forms. Method of soil analysis. Part 2. Chemical and microbiological properties. Agronomy 9:643–698Google Scholar
  30. Könneke M, Bernhard AE, José R, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature, 437:543–546Google Scholar
  31. Laanbroek HJ (1990) Bacterial cycling of minerals that affect plant growth in waterlogged soils: a review. Aquat Bot 38:109–125CrossRefGoogle Scholar
  32. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol G, Prosser J, Schuster S, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809CrossRefPubMedGoogle Scholar
  33. Liu YR, Delgado-Baquerizo M, Trivedi P, He JZ, Singh BK (2016) Species identity of biocrust-forming lichens drives the response of soil nitrogen cycle to altered precipitation frequency and nitrogen amendment. Soil Biol Biochem 96:128–136CrossRefGoogle Scholar
  34. Long A, Heitman J, Tobias C, Philips R, Song B (2013) Co-occurring anammox, denitrification, and codenitrification in agricultural soils. Appl Environ Microbiol 79:168–176CrossRefPubMedPubMedCentralGoogle Scholar
  35. Lu S, Tang C, Rengel Z (2004) Combined effects of waterlogging and salinity on electrochemistry, water-soluble cations and water dispersible clay in soils with various salinity levels. Plant Soil 264:231–245CrossRefGoogle Scholar
  36. McCauley A, Jones C, Jacobsen J (2009) Soil pH and organic matter. Nutrient Management Module 8:1–12Google Scholar
  37. Milroy SP, Bange MP, Thongbai P (2009) Cotton leaf nutrient concentrations in response to waterlogging under field conditions. Field Crop Res 113:246–255CrossRefGoogle Scholar
  38. Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10:2966–2978CrossRefPubMedGoogle Scholar
  39. Northcote KH, Hubble G, Isbell R, Thompson C, Bettenay E (1975) A description of Australian soils. Melbourne, CSIROGoogle Scholar
  40. Offre P, Kerou M, Spang A, Schleper C (2014) Variability of the transporter gene complement in ammonia-oxidizing archaea. Trends Microbiol 22:665–675CrossRefPubMedGoogle Scholar
  41. Patrick WH, Reddy KR (1976) Nitrification-denitrification reactions in flooded soils and water bottoms: dependence on oxygen supply and ammonium diffusion. J Environ Qual 5:469–472CrossRefGoogle Scholar
  42. Reddy KR and Patrick WH (1975) Effect of alternate aerobic and anaerobic conditions on redox potential, organic matter decomposition and nitrogen loss in a flooded soil. Soil Biol Biochem 7:87–94CrossRefGoogle Scholar
  43. Rochester I, Constable G (2015) Improvements in nutrient uptake and nutrient use-efficiency in cotton cultivars released between 1973 and 2006. Field Crop Res 173:14–21CrossRefGoogle Scholar
  44. Rochester I, Constable G, Macleod D (1993) Cycling of fertilizer and cotton crop residue nitrogen. Soil Res 31:597–609CrossRefGoogle Scholar
  45. Rochester I, Gaynor H, Constable G, Saffigna P (1994) Etridiazole may conserve applied nitrogen and increase yield of irrigated cotton. Soil Res 32:1287–1300CrossRefGoogle Scholar
  46. Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712PubMedPubMedCentralGoogle Scholar
  47. Sahay R (1989) Photosynthetic and stomatal responses of cotton to drought stress and waterlogging. Agric Sci Dig 9:198–200Google Scholar
  48. Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394CrossRefPubMedGoogle Scholar
  49. Singh BK, Bardgett RD, Smith P, Reay DS (2010) Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nat Rev Microbiol 8:779–790CrossRefPubMedGoogle Scholar
  50. Sterngren AE, Hallin S, Bengtson P (2015) Archaeal ammonia oxidizers dominate in numbers, but bacteria drive gross nitrification in N-amended grassland soil. Front Microbiol 6:1350CrossRefPubMedPubMedCentralGoogle Scholar
  51. Szukics U, Hackl E, Zechmeister-Boltenstern S, Sessitsch A (2012) Rapid and dissimilar response of ammonia oxidizing archaea and bacteria to nitrogen and water amendment in two temperate forest soils. Microbiol Res 167:103–109CrossRefPubMedGoogle Scholar
  52. Tourna M, Freitag TE, Nicol GW, Prosser JI (2008) Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol 10:1357–1364CrossRefPubMedGoogle Scholar
  53. Van Schreven D, Sieben W (1972) The effect of storage of soils under water-logged conditions upon subsequent mineralization of nitrogen, nitrification and fixation of ammonia. Plant Soil 37:245–253CrossRefGoogle Scholar
  54. Wang FL, Bettany JR (1994) Organic and inorganic nitrogen leaching from incubated soils subjected to freeze-thaw and flooding conditions. Can J Soil Sci 74:201–206CrossRefGoogle Scholar
  55. Xia W, Zhang C, Zeng X, Feng Y, Weng J, Lin X, Zhu J, Xiong Z, Xu J, Cai Z (2011) Autotrophic growth of nitrifying community in an agricultural soil. ISME J 5:1226–1236CrossRefPubMedPubMedCentralGoogle Scholar
  56. Yao H, Gao Y, Nico GW, Campbell CD, Prosser JI, Zhang L, Han W, Singh BK (2011) Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl Envrion Microbiol 77:4618–4625CrossRefGoogle Scholar
  57. 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 6:1032–1045CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Linh T. T. Nguyen
    • 1
  • Yui Osanai
    • 1
    • 2
  • Ian C. Anderson
    • 1
  • Michael P. Bange
    • 3
  • Michael Braunack
    • 3
  • David T. Tissue
    • 1
  • Brajesh K. Singh
    • 1
    • 4
  1. 1.Hawkesbury Institute for the EnvironmentWestern Sydney UniversityPenrithAustralia
  2. 2.School of Environmental and Rural SciencesUniversity of New EnglandArmidaleAustralia
  3. 3.CSIRO Agriculture and FoodAustralian Cotton Research InstituteNarrabriAustralia
  4. 4.Global Centre for Land-Based InnovationWestern Sydney UniversityPenrithAustralia

Personalised recommendations