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Intensive Management Affects Composition of Betaproteobacterial Ammonia Oxidizers in Turfgrass Systems

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Abstract

Turfgrass is a highly managed ecosystem subject to frequent fertilization, mowing, irrigation, and application of pesticides. Turf management practices may create a perturbed environment for ammonia oxidizers, a key microbial group responsible for nitrification. To elucidate the long-term effects of turf management on these bacteria, we assessed the composition of betaproteobacterial ammonia oxidizers in a chronosequence of turfgrass systems (i.e., 1, 6, 23, and 95 years old) and the adjacent native pines by using both 16S rRNA and amoA gene fragments specific to ammonia oxidizers. Based on the Shannon–Wiener diversity index of denaturing gradient gel electrophoresis patterns and the rarefaction curves of amoA clones, turf management did not change the relative diversity and richness of ammonia oxidizers in turf soils as compared to native pine soils. Ammonia oxidizers in turfgrass systems comprised a suite of phylogenetic clusters common to other terrestrial ecosystems. Nitrosospira clusters 0, 2, 3, and 4; Nitrosospira sp. Nsp65-like sequences; and Nitrosomonas clusters 6 and 7 were detected in the turfgrass chronosequence with Nitrosospira clusters 3 and 4 being dominant. However, both turf age and land change (pine to turf) effected minor changes in ammonia oxidizer composition. Nitrosospira cluster 0 was observed only in older turfgrass systems (i.e., 23 and 95 years old); fine-scale differences within Nitrosospira cluster 3 were seen between native pines and turf. Further investigations are needed to elucidate the ecological implications of the compositional differences.

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References

  1. Aakra A, Utåker JB, Nes IF (2001) Comparative phylogeny of the ammonia monooxygenase subunit A and 16S rRNA genes of ammonia-oxidizing bacteria. FEMS Microbiol Lett 205:237–242

    Article  PubMed  CAS  Google Scholar 

  2. Avrahami S, Liesack W, Conrad R (2003) Effects of temperature and fertilizer on activity and community structure of soil ammonia oxidizers. Environ Microbiol 5:691–705

    Article  PubMed  CAS  Google Scholar 

  3. Bäckman JS, Hermansson A, Tebbe CC, Lindgren P-E (2003) Liming induces growth of a diverse flora of ammonia-oxidising bacteria in acid spruce forest soil as determined by SSCP and DGGE. Soil Biol Biochem 35:1337–1347

    Article  CAS  Google Scholar 

  4. Bollmann A, Bär-Gilissen MJ, Laanbroek HJ (2002) Growth at low ammonium concentrations and starvation response as potential factors involved in niche differentiation among ammonia-oxidizing bacteria. Appl Environ Microbiol 68:4751–4757

    Article  PubMed  CAS  Google Scholar 

  5. Bruns MA, Stephen JR, Kowalchuk GA, Prosser JI, Paul EA (1999) Comparative diversity of ammonia oxidizer 16S rRNA gene sequences in native, tilled, and successional soils. Appl Environ Microbiol 65:2994–3000

    PubMed  CAS  Google Scholar 

  6. Carney KM, Matson PA, Bohannan BM (2004) Diversity and composition of tropical soil nitrifiers across a plant diversity gradient and among land-use types. Ecol Lett 7:684–694

    Article  Google Scholar 

  7. Cébron A, Coci M, Garnier J, Laanbroek HJ (2004) Denaturing gradient gel electrophoretic analysis of ammonia-oxidizing bacterial community structure in the lower Seine river: impact of Paris wastewater effluents. Appl Environ Microbiol 70:6726–6737

    Article  PubMed  CAS  Google Scholar 

  8. Chang Y-J, Hussain A, Stephen JR, Mullen MD, White DC, Peacock A (2001) Impact of herbicides on the abundance and structure of indigenous β-subgroup ammonia-oxidizer communities in soil microcosms. Environ Toxicol Chem 20:2462–2468

    Article  PubMed  CAS  Google Scholar 

  9. Gafan GP, Spratt DA (2005) Denaturing gradient gel electrophoresis gel expansion (DGGEGE)-an attempt to resolve the limitations of co-migration in the DGGE of complex polymicrobial communities. FEMS Microbiol Lett 253:303–307

    Article  PubMed  CAS  Google Scholar 

  10. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  11. Hawkes CV, Wren IF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985

    Article  Google Scholar 

  12. Head IM, Hiorns WD, Embley TM, McCarthy AJ, Saunders JR (1993) The phylogeny of autotrophic ammonia-oxidizing bacteria determined by analysis of 16S ribosomal RNA gene sequences. J Gen Microbiol 139:1147–1153

    PubMed  CAS  Google Scholar 

  13. Jiang QQ, Bakken LR (1999) Nitrous oxide production and methane oxidation by different ammonia-oxidizing bacteria. Appl Environ Microbiol 65:2679–2684

    PubMed  CAS  Google Scholar 

  14. Jones TH, Bradford MA (2001) Assessing the functional implications of soil biodiversity in ecosystems. Ecol Res 16:845–858

    Article  Google Scholar 

  15. Koops HP, Purkhold U, Pommerening-Röser A, Timmermann G, Wagner M (2003) The lithotrophic ammonia oxidizing bacteria. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes: an evolving electronic resource for the microbiological community, 3rd edn. Springer, New York http://link.springerny.com/link/service/books/10125/

    Google Scholar 

  16. Kowalchuk GA, Stephen JR, De Boer W, Prosser JL, Embley TM, Woldendorp JW (1997) Analysis of ammonia-oxidizing bacteria of the beta subdivision of the class Proteobacteria in coastal sand dunes by denaturing gradient gel electrophoresis and sequencing of PCR-amplified 16S ribosomal DNA fragments. Appl Environ Microbiol 63:1489–1497

    PubMed  CAS  Google Scholar 

  17. Kowalchuk GA, Steinstra AW, Heilig GH, Stephen JR, Woldendorp JW (2000) Changes in the community structure of ammonia-oxidizing bacteria during secondary succession of calcareous grasslands. Environ Microbiol 2:99–110

    Article  PubMed  CAS  Google Scholar 

  18. Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529

    Article  PubMed  CAS  Google Scholar 

  19. Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  20. Laverman AM, Speksnijder AG, Braster M, Kowalchuk GA, Verhoef HA, Van Verseveld HW (2001) Spatio-temporal stability of an ammonia oxidizing community in a nitrogen-saturated forest soil. Microbial Ecol 42:35–45

    CAS  Google Scholar 

  21. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809

    Article  PubMed  CAS  Google Scholar 

  22. Low AP, Stark JM, Dudley LM (1997) Effects of soil osmotic potential on nitrification, ammonification, N-assimilation, and nitrous oxide production. Soil Sci 162:16–27

    Article  CAS  Google Scholar 

  23. McCaig AE, Embley TM, Prosser JI (1994) Molecular analysis of enrichment cultures of marine ammonia oxidizers. FEMS Microbiol Lett 120:363–368

    Article  PubMed  CAS  Google Scholar 

  24. McTavish H, Fuchs JA, Hooper AB (1993) Sequence of the gene coding for ammonia monooxygenase in Nitrosomonas europaea. J Bacteriol 175:2436–2444

    PubMed  CAS  Google Scholar 

  25. Milesi C, Running SW, Elvidge CD, Dietz JB, Tuttle BJ, Nemani RR (2005) Mapping and modeling the biogeochemical cycling of turf grasses in the United States. Environ Manage 36:426–438

    Article  PubMed  Google Scholar 

  26. Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    PubMed  CAS  Google Scholar 

  27. Nicolaisen MH, Ramsing NB (2002) Denaturing gradient gel electrophoresis (DGGE) approaches to study the diversity of ammonia-oxidizing bacteria. J Microbiol Methods 50:189–203

    Article  PubMed  CAS  Google Scholar 

  28. Norton JM, Low JM, Klotz MG (1996) The gene encoding ammonia monooxygenase subunit A exists in three nearly identical copies in Nitrosospira sp. NpAV. FEMS Microbiol Lett 139:181–188

    PubMed  CAS  Google Scholar 

  29. Nugroho RA, Röling WFM, Laverman AM, Verhoef HA (2007) Low nitrification rates in acid Scots pine forest soils are due to pH-related factors. Microb Ecol 53:89–97

    Article  PubMed  CAS  Google Scholar 

  30. Oved T, Shaviv A, Goldrath T, Mandelbaum RT, Minz D (2001) Influence of effluent irrigation on community composition and function of ammonia-oxidizing bacteria in soil. Appl Environ Microbiol 67:3426–3433

    Article  PubMed  CAS  Google Scholar 

  31. Phillips CJ, Harris D, Dollhopf SL, Gross KL, Prosser JI, Paul EA (2000) Effects of agronomic treatments on structure and function of ammonia-oxidizing communities. Appl Environ Microbiol 66:5410–5418

    Article  PubMed  CAS  Google Scholar 

  32. Purkhold U, Pommerening-Röser A, Juretschko S, Schmid MC, Koops HP, Wagner M (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environ Microbiol 66:5368–5382

    Article  PubMed  CAS  Google Scholar 

  33. Purkhold U, Wagner M, Timmermann G, Pommerening-Röser A, Koops HP (2003) 16S rRNA and amoA-based phylogeny of 12 novel betaproteobacterial ammonia-oxidizing isolates: extension of the dataset and proposal of a new lineage within the nitrosomonads. Int J Syst Evol Microbiol 53:1485–1494

    Article  PubMed  CAS  Google Scholar 

  34. Risgaard-Petersen N, Nicolaisen MH, Revsbech NP, Lomstein BA (2004) Competition between ammonia-oxidizing bacteria and benthic microalgae. Appl Environ Microbiol 70:5528–5537

    Article  PubMed  CAS  Google Scholar 

  35. Schloss PD, Handelsman J (2004) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506

    Article  CAS  Google Scholar 

  36. Shi W, Yao H, Bowman D (2006a) Soil microbial biomass, activity and nitrogen transformations in a turfgrass chronosequence. Soil Biol Biochem 38:311–319

    Article  CAS  Google Scholar 

  37. Shi W, Muruganandam S, Bowman D (2006b) Soil microbial biomass and nitrogen dynamics in a turfgrass chronosequence: a short-term response to turfgrass clipping addition. Soil Biol Biochem 38:2032–2042

    Article  CAS  Google Scholar 

  38. Stark JM, Firestone MK (1996) Kinetic characteristics of ammonium-oxidizer communities in a California oak woodland-annual grassland. Soil Biol Biochem 28:1307–1317

    Article  CAS  Google Scholar 

  39. Stephen JR, McCaig AE, Smith Z, Prosser JI, Embley TM (1996) Molecular diversity of soil and marine 16S rDNA sequences related to b-subgroup ammonia-oxidizing bacteria. Appl Environ Microbiol 62:4147–4154

    PubMed  CAS  Google Scholar 

  40. Stephen JR, Kowalchuk GA, Bruns MAV, McCaig AE, Phillips CJ, Embley TM, Prosser JI (1998) Analysis of β-subgroup proteobacterial ammonia oxidizer populations in soil by denaturing gradient gel electrophoresis analysis and hierarchical phylogenetic probing. Appl Environ Microbiol 64:2958–2965

    PubMed  CAS  Google Scholar 

  41. Thompson JR, Marcelino LA, Polz MF (2002) Heteroduplexes in mixed-template amplifications: formation, consequence and elimination by reconditioning PCR. Nucleic Acids Res 30:2083–2088

    Article  PubMed  CAS  Google Scholar 

  42. Torsvik V, Ovreas L, Thingstad TF (2002) Prokaryotic diversity—magnitude, dynamics, and controlling factors. Science 296:1064–1066

    Article  PubMed  CAS  Google Scholar 

  43. Webster G, Embley TM, Prosser JI (2002) Grassland management regimens reduce small-scale heterogeneity and species diversity of proteobacterial ammonia oxidizer populations. Appl Environ Microbiol 68:20–30

    Article  PubMed  CAS  Google Scholar 

  44. Webster G, Embley TM, Freitag TE, Smith Z, Prosser JI (2005) Links between ammonia oxidizer species composition, functional diversity and nitrification kinetics in grassland soils. Environ Microbiol 7:676–684

    Article  PubMed  CAS  Google Scholar 

  45. Yao H, Bowman D, Shi W (2006) Soil microbial community structure and diversity in a turfgrass chronosequence: land-use change versus turfgrass management. Appl Soil Ecol 34:209–218

    Article  Google Scholar 

  46. Yeager CM, Northup DE, Grow CC, Barns SM, Kuske CR (2005) Changes in nitrogen-fixing and ammonia-oxidizing bacterial communities in soil of a mixed conifer forest after wildfire. Appl Environ Microbiol 71:2713–2722

    Article  PubMed  CAS  Google Scholar 

  47. Zhang X, Yan X, Gao P, Wang L, Zhou Z, Zhao L (2005) Optimized sequence retrieval from single bands of temperature gradient gel electrophoresis profiles of the amplified 16S rDNA fragments from an activated sludge system. J Microbiol Methods 60:1–11

    Article  PubMed  CAS  Google Scholar 

  48. Zhou J, Xia B, Treves DS, Wu LY, Marsh TL, O’Neill RV, Palumbo AV, Tiedje JM (2002) Spatial and resource factors influencing high microbial diversity in soil. Appl Environ Microbiol 68:326–334

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This study was supported financially by the Center for Turfgrass Research and Education at North Carolina State University. We thank Drs. Rongda Qu and Sivamani Elumalai for their suggestions and comments on DNA hybridization and thank the Pinehurst Resort and Country Club and Forest Creek Golf Club for allowing us to take soil samples from their golf courses. Two anonymous reviewers provided constructive comments to improve the manuscript.

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Correspondence to Wei Shi.

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Dell, E.A., Bowman, D., Rufty, T. et al. Intensive Management Affects Composition of Betaproteobacterial Ammonia Oxidizers in Turfgrass Systems. Microb Ecol 56, 178–190 (2008). https://doi.org/10.1007/s00248-007-9335-x

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