Seasonal Patterns in Microbial Community Composition in Denitrifying Bioreactors Treating Subsurface Agricultural Drainage

Abstract

Denitrifying bioreactors, consisting of water flow control structures and a woodchip-filled trench, are a promising approach for removing nitrate from agricultural subsurface or tile drainage systems. To better understand the seasonal dynamics and the ecological drivers of the microbial communities responsible for denitrification in these bioreactors, we employed microbial community “fingerprinting” techniques in a time-series examination of three denitrifying bioreactors over 2 years, looking at bacteria, fungi, and the denitrifier functional group responsible for the final step of complete denitrification. Our analysis revealed that microbial community composition responds to depth and seasonal variation in moisture content and inundation of the bioreactor media, as well as temperature. Using a geostatistical analysis approach, we observed recurring temporal patterns in bacterial and denitrifying bacterial community composition in these bioreactors, consistent with annual cycling. The fungal communities were more stable, having longer temporal autocorrelations, and did not show significant annual cycling. These results suggest a recurring seasonal cycle in the denitrifying bioreactor microbial community, likely due to seasonal variation in moisture content.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. 1.

    Schipper LA, Robertson WD, Gold AJ, Jaynes DB, Cameron SC (2010) Denitrifying bioreactors—an approach for reducing nitrate loads to receiving waters. Ecol Eng 36:1532–1543. doi:10.1016/J.Ecoleng.2010.04.008

    Article  Google Scholar 

  2. 2.

    Blann KL, Anderson JL, Sands GR, Vondracek B (2009) Effects of agricultural drainage on aquatic ecosystems: a review. Crit Rev Environ Sci Technol 39:909–1001. doi:10.1080/10643380801977966

    CAS  Article  Google Scholar 

  3. 3.

    Dinnes DL, Karlen DL, Jaynes DB, Kaspar TC, Hatfield JL, Colvin TS, Cambardella CA (2002) Nitrogen management strategies to reduce nitrate leaching in tile-drained Midwestern soils. Agron J 94:153–171

    Article  Google Scholar 

  4. 4.

    Cameron SG, Schipper LA (2010) Nitrate removal and hydraulic performance of organic carbon for use in denitrification beds. Ecol Eng 36:1588–1595. doi:10.1016/J.Ecoleng.2010.03.010

    Article  Google Scholar 

  5. 5.

    Greenan CM, Moorman TB, Kaspar TC, Parkin TB, Jaynes DB (2006) Comparing carbon substrates for denitrification of subsurface drainage water. J Environ Qual 35:824–829. doi:10.2134/Jeq2005.0247

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Chun JA, Cooke RA, Eheart JW, Cho J (2010) Estimation of flow and transport parameters for woodchip-based bioreactors: II. Field-scale bioreactor. Biosyst Eng 105:95–102. doi:10.1016/J.Biosystemseng.2009.09.018

    Article  Google Scholar 

  7. 7.

    Christianson L, Helmers M, Bhandari A, Moorman T (2013) Internal hydraulics of an agricultural drainage denitrification bioreactor. Ecol Eng 52:298–307. doi:10.1016/J.Ecoleng.2012.11.001

    Article  Google Scholar 

  8. 8.

    Long LM, Schipper LA, Bruesewitz DA (2011) Long-term nitrate removal in a denitrification wall. Agric Ecosyst Environ 140:514–520. doi:10.1016/J.Agee.2011.02.005

    CAS  Article  Google Scholar 

  9. 9.

    Moorman TB, Parkin TB, Kaspar TC, Jaynes DB (2010) Denitrification activity, wood loss, and N2O emissions over 9 years from a wood chip bioreactor. Ecol Eng 36:1567–1574. doi:10.1016/J.Ecoleng.2010.03.012

    Article  Google Scholar 

  10. 10.

    Robertson WD, Ptacek CJ, Brown SJ (2009) Rates of nitrate and perchlorate removal in a 5-year-old wood particle reactor treating agricultural drainage. Ground Water Monit Remediat 29:87–94. doi:10.1111/J.1745-6592.2009.01231.X

    CAS  Article  Google Scholar 

  11. 11.

    Warneke S, Schipper LA, Bruesewitz DA, McDonald I, Cameron S (2011) Rates, controls and potential adverse effects of nitrate removal in a denitrification bed. Ecol Eng 37:511–522. doi:10.1016/j.ecoleng.2010.12.006

    Article  Google Scholar 

  12. 12.

    Warneke S, Schipper LA, Matiasek MG, Scow KM, Cameron S, Bruesewitz DA, McDonald IR (2011) Nitrate removal, communities of denitrifiers and adverse effects in different carbon substrates for use in denitrification beds. Water Res 45:5463–5475. doi:10.1016/J.Watres.2011.08.007

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  13. 13.

    Andrus JM, Porter MD, Rodríguez LF, Kuehlhorn T, Cooke RAC, Zhang Y, Kent AD, Zilles JL (2014) Spatial variation in the bacterial and denitrifying bacterial community in a biofilter treating subsurface agricultural drainage. Microb Ecol 67:265–272

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Cooke R, Verma S (2012) Performance of drainage water management systems in Illinois, United States. J Soil Water Conserv 67:453–464. doi:10.2489/Jswc.67.6.453

    Article  Google Scholar 

  15. 15.

    Woli KP, David MB, Cooke RA, McIsaac GF, Mitchell CA (2010) Nitrogen balance in and export from agricultural fields associated with controlled drainage systems and denitrifying bioreactors. Ecol Eng 36:1558–1566. doi:10.1016/J.Ecoleng.2010.04.024

    Article  Google Scholar 

  16. 16.

    Seitzinger S, Harrison JA, Bohlke JK, Bouwman AF, Lowrance R, Peterson B, Tobias C, Van Drecht G (2006) Denitrification across landscapes and waterscapes: a synthesis. Ecol Appl 16:2064–2090. doi:10.1890/1051-0761(2006)016[2064:Dalawa]2.0.Co;2

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Wallenstein MD, Myrold DD, Firestone M, Voytek M (2006) Environmental controls on denitrifying communities and denitrification rates: insights from molecular methods. Ecol Appl 16:2143–2152. doi:10.1890/1051-0761(2006)016[2143:Ecodca]2.0.Co;2

    Article  PubMed  Google Scholar 

  18. 18.

    Smith J, Wagner-Riddle C, Dunfield K (2010) Season and management related changes in the diversity of nitrifying and denitrifying bacteria over winter and spring. Appl Soil Ecol 44:138–146. doi:10.1016/J.Apsoil.2009.11.004

    Article  Google Scholar 

  19. 19.

    Laughlin RJ, Stevens RJ (2002) Evidence for fungal dominance of denitrification and codenitrification in a grassland soil. Soil Sci Soc Am J 66:1540–1548

    CAS  Article  Google Scholar 

  20. 20.

    Long A, Heitman J, Tobias C, Philips R, Song B (2013) Co-occuring anammox, denitrification, and codenitrification in agricultural soils. Appl Environ Microbiol 79:168–176. doi:10.1128/AEM. 02520-12

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  21. 21.

    Sanford RA, Wagner DD, Wu Q, Chee-Sanford JC, Thomas SH, Cruz-Garcia C, Rodriguez G, Massol-Deya A, Krishnani KK, Ritalahti KM, Nissen S, Konstantinidis KT, Loffler FE (2012) Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proc Natl Acad Sci U S A 109:19709–19714. doi:10.1073/pnas.1211238109

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  22. 22.

    Jones CM, Graf DR, 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. doi:10.1038/ismej.2012.125

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  23. 23.

    Appleford JM, Rodriguez LF, Cooke RAC, Zhang Y, Kent AD, Zilles J (2008) Characterization of microorganisms contributing to denitrification in tile train biofilters in Illinois. Proceedings of the 2008 ASABE Annual International Meeting, Providence, RI, paper no. 084583, pp 5605-5614

  24. 24.

    Crump BC, Hobbie JE (2005) Synchrony and seasonality in bacterioplankton communities of two temperate rivers. Limnol Oceanogr 50:1718–1729

    CAS  Article  Google Scholar 

  25. 25.

    Fuhrman JA, Hewson I, Schwalbach MS, Steele JA, Brown MV, Naeem S (2006) Annually reoccurring bacterial communities are predictable from ocean conditions. Proc Natl Acad Sci U S A 103:13104–13109. doi:10.1073/Pnas.0602399103

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  26. 26.

    Jones SE, Shade AL, McMahon KD, Kent AD (2007) Comparison of primer sets for use in automated ribosomal intergenic spacer analysis of aquatic bacterial communities: an ecological perspective. Appl Environ Microbiol 73:659–662. doi:10.1128/Aem. 02130-06

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  27. 27.

    Kent AD, Jones SE, Yannarell AC, Graham JM, Lauster GH, Kratz TK, Triplett EW (2004) Annual patterns in bacterioplankton community variability in a humic lake. Microb Ecol 48:550–560. doi:10.1007/s00248-004-0244-y

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Nelson CE (2009) Phenology of high-elevation pelagic bacteria: the roles of meteorologic variability, catchment inputs and thermal stratification in structuring communities. ISME J 3:13–30. doi:10.1038/Ismej.2008.81

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Shade A, Kent AD, Jones SE, Newton RJ, Triplett EW, McMahon KD (2007) Interannual dynamics and phenology of bacterial communities in a eutrophic lake. Limnol Oceanogr 52:487–494

    CAS  Article  Google Scholar 

  30. 30.

    Lauber CL, Ramirez KS, Aanderud Z, Lennon J, Fierer N (2013) Temporal variability in soil microbial communities across land-use types. ISME J 7:1641–1650. doi:10.1038/Ismej.2013.50

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  31. 31.

    Boer SI, Hedtkamp SIC, van Beusekom JEE, Fuhrman JA, Boetius A, Ramette A (2009) Time- and sediment depth-related variations in bacterial diversity and community structure in subtidal sands. ISME J 3:780–791. doi:10.1038/Ismej.2009.29

    Article  PubMed  Google Scholar 

  32. 32.

    Song K, Lee SH, Kong H (2011) Denitrification rates and community structure of denitrifying bacteria in newly constructed wetland. Eur J Soil Biol 47:24–29. doi:10.1016/J.Ejsobi.2010.10.003

    CAS  Article  Google Scholar 

  33. 33.

    Gobet A, Boetius A, Ramette A (2014) Ecological coherence of diversity patterns derived from classical fingerprinting and Next Generation Sequencing techniques. Environ Microbiol 16:2672–2681. doi:10.1111/1462-2920.12308

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  34. 34.

    van Dorst J, Bissett A, Palmer AS, Brown M, Snape I, Stark JS, Raymond B, McKinlay J, Ji M, Winsley T, Ferrari BC (2014) Community fingerprinting in a sequencing world. FEMS Microbiol Ecol 89:316–330. doi:10.1111/1574-6941.12308

    Article  PubMed  Google Scholar 

  35. 35.

    Andrus JM (2011) Microbial community analysis for denitrifying biofilters. PhD dissertation, University of Illinois at Urbana-Champagin. http://hdl.handle.net/2142/24094

  36. 36.

    Peralta AL, Matthews JW, Kent AD (2010) Microbial community structure and denitrification in a wetland mitigation bank. Appl Environ Microbiol 76:4207–4215. doi:10.1128/Aem. 02977-09

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  37. 37.

    Kent AD, Yannarell AC, Rusak JA, Triplett EW, McMahon KD (2007) Synchrony in aquatic microbial community dynamics. ISME J 1:38–47. doi:10.1038/Ismej.2007.6

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Ranjard L, Poly F, Lata JC, Mougel C, Thioulouse J, Nazaret S (2001) Characterization of bacterial and fungal soil communities by automated ribosomal intergenic spacer analysis fingerprints: biological and methodological variability. Appl Environ Microbiol 67:4479–4487

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  39. 39.

    Rich JJ, Heichen RS, Bottomley PJ, Cromack K, Myrold DD (2003) Community composition and functioning of denitrifying bacteria from adjacent meadow and forest soils. Appl Environ Microbiol 69:5974–5982. doi:10.1128/Aem. 69.10.5974-5982.2003

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  40. 40.

    Yannarell AC, Triplett EW (2005) Geographic and environmental sources of variation in lake bacterial community composition. Appl Environ Microbiol 71:227–239. doi:10.1128/Aem. 71.1.227-239.2005

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  41. 41.

    Rees G, Baldwin D, Watson G, Perryman S, Nielsen D (2004) Ordination and significance testing of microbial community composition derived from terminal restriction fragment length polymorphisms: application of multivariate statistics. Anton Leeuw Int J G 86:339–347. doi:10.1007/s10482-004-0498-x

    Article  Google Scholar 

  42. 42.

    terBraak CJF, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Wageningen University and Research Center Publications, City, p 500

    Google Scholar 

  43. 43.

    Clarke KR (1993) Nonparametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  44. 44.

    Clarke KR, Green RH (1988) Statistical design and analysis for a biological effects study. Mar Ecol Prog Ser 46:213–226

    Article  Google Scholar 

  45. 45.

    Legendre P, Legendre L (1998) Numerical ecology. Elsevier Science, Amsterdam

    Google Scholar 

  46. 46.

    Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:326–349

    Article  Google Scholar 

  47. 47.

    Oden NL, Sokal RR (1986) Directional autocorrelation—an extension of spatial correlograms to 2 dimensions. Syst Zool 35:608–617

    Article  Google Scholar 

  48. 48.

    Legendre P (1993) Spatial autocorrelation: trouble or new paradigm? Ecology 74:1659–1673. doi:10.2307/1939924

    Article  Google Scholar 

  49. 49.

    Sexstone AJ, Parkin TB, Tiedje JM (1985) Temporal response of soil dentrification rates to rainfall and irrigation. Soil Sci Soc Am J 49:99–103

    CAS  Article  Google Scholar 

  50. 50.

    Shade A, Jones SE, McMahon KD (2008) The influence of habitat heterogeneity on freshwater bacterial community composition and dynamics. Environ Microbiol 10:1057–1067. doi:10.1111/J.1462-2920.2007.01527.X

    CAS  Article  PubMed  Google Scholar 

  51. 51.

    Peralta AL, Matthews JW, Kent AD (2014) Habitat specialization along a wetland moisture gradient differs between ammonia-oxidizing and denitrifying microorganisms. Microb Ecol 68:339–350. doi:10.1007/s00248-014-0407-4

    CAS  Article  PubMed  Google Scholar 

  52. 52.

    Krave AS, Lin B, Braster M, Laverman AM, van Straalen NM, Roling WFM, van Verseveld HW (2002) Stratification and seasonal stability of diverse bacterial communities in a Pinus merkusii (pine) forest soil in central Java, Indonesia. Environ Microbiol 4:361–373

    Article  PubMed  Google Scholar 

  53. 53.

    Lejon DPH, Chaussod R, Ranger J, Ranjard L (2005) Microbial community structure and density under different tree species in an acid forest soil (Morvan, France). Microb Ecol 50:614–625. doi:10.1007/S00248-005-5130-8

    Article  PubMed  Google Scholar 

  54. 54.

    Goberna M, Insam H, Klammer S, Pascual JA, Sanchez J (2005) Microbial community structure at different depths in disturbed and undisturbed semiarid Mediterranean forest soils. Microb Ecol 50:315–326

    CAS  Article  PubMed  Google Scholar 

  55. 55.

    Drenovsky RE, Vo D, Graham KJ, Scow KM (2004) Soil water content and organic carbon availability are major determinants of soil microbial community composition. Microb Ecol 48:424–430. doi:10.1007/S00248-003-1063-2

    CAS  Article  PubMed  Google Scholar 

  56. 56.

    Kent AD, Jones SE, Yannarell AC, Graham JM, Lauster GH, Kratz TK, Triplett EW (2004) Annual patterns in bacterioplankton community variability in a humic lake. Microb Ecol 48:550–560

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful for technical assistance provided by D. Kimme for analysis of nitrate concentrations in water and for assistance from A.L. Peralta and S.F. Paver in microbial ecology laboratory techniques. R.A.C. Cooke and S. Vermakindly provided bioreactor design information, as well as flow and performance data. Funding was provided by a US Department of Agriculture National Needs Fellowship to J.M.A. and by US National Science Foundation project CBET-0853820.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Angela D. Kent.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 7406 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Porter, M.D., Andrus, J.M., Bartolerio, N.A. et al. Seasonal Patterns in Microbial Community Composition in Denitrifying Bioreactors Treating Subsurface Agricultural Drainage. Microb Ecol 70, 710–723 (2015). https://doi.org/10.1007/s00248-015-0605-8

Download citation

Keywords

  • Denitrification
  • Geostatistics
  • Nitrate removal
  • Seasonal variation
  • Subsurface drainage