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Impact of Land Use Management and Soil Properties on Denitrifier Communities of Namibian Savannas

  • Soil Microbiology
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Abstract

We studied potential denitrification activity and the underlying denitrifier communities in soils from a semiarid savanna ecosystem of the Kavango region in NE Namibia to help in predicting future changes in N2O emissions due to continuing changes of land use in this region. Soil type and land use (pristine, fallow, and cultivated soils) influenced physicochemical characteristics of the soils that are relevant to denitrification activity and N2O fluxes from soils and affected potential denitrification activity. Potential denitrification activity was assessed by using the denitrifier enzyme activity (DEA) assay as a proxy for denitrification activity in the soil. Soil type and land use influenced C and N contents of the soils. Pristine soils that had never been cultivated had a particularly high C content. Cultivation reduced soil C content and the abundance of denitrifiers and changed the composition of the denitrifier communities. DEA was strongly and positively correlated with soil C content and was higher in pristine than in fallow or recently cultivated soils. Soil type and the composition of both the nirK- and nirS-type denitrifier communities also influenced DEA. In contrast, other soil characteristics like N content, C:N ratio, and pH did not predict DEA. These findings suggest that due to greater availability of soil organic matter, and hence a more effective N cycling, the natural semiarid grasslands emit more N2O than managed lands in Namibia.

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References

  1. Crutzen PJ (1970) The influence of nitrogen oxides on the atmospheric ozone content. Q J R Meteorol Soc 96:320–325

    Article  Google Scholar 

  2. IPCC (2001) Climate change 2001: a scientific basis. Intergovernmental panel on climate change. Cambridge University Press, Cambridge

    Google Scholar 

  3. EPA (2010) Methane and nitrous oxide emissions from natural sources, Inventory of U.S. greenhouse gas emissions and sinks: 1990–2008. U.S. Environmental Protection Agency, Washington, pp 1–194

    Google Scholar 

  4. Bhandral R, Saggar S, Bolan NS, Hedley MJ (2007) Transformation of nitrogen and nitrous oxide emission from grassland soils as affected by compaction. Soil Tillage Res 94:482–492. doi:10.1016/j.still.2006.10.006

    Article  Google Scholar 

  5. Gärdenäs AI, Ågren GI, Bird JA, Clarholm M, Hallin S, Ineson P et al (2011) Knowledge gaps in soil carbon and nitrogen interactions—from molecular to global scale. Soil Biol Biochem 43:702–717. doi:10.1016/j.soilbio.2010.04.006

    Article  Google Scholar 

  6. Burger M, Jackson LE (2003) Microbial immobilization of ammonium and nitrate in relation to ammonification and nitrification rates in organic and conventional cropping systems. Soil Biol Biochem 35:29–36. doi:10.1016/S0038-0717(02)00233-X

    Article  CAS  Google Scholar 

  7. Rafique R, Hennessy D, Kiely G (2011) Nitrous oxide emission from grazed grassland under different management systems. Ecosystems 14:563–582. doi:10.1007/s10021-011-9434-x9

    Article  CAS  Google Scholar 

  8. Castaldi S, Ermice A, Strumia S (2006) Fluxes of N2O and CH4 from soils of savannas and seasonally-dry ecosystems. J Biogeogr 33:401–415. doi:10.1111/j.1365-2699.2005.01447.x

    Article  Google Scholar 

  9. Hickman JE, Havlikova M, Kroeze C, Palm CA (2011) Current and future nitrous oxide emissions from African agriculture. Curr Opin Environ Sustain 3:370–378. doi:10.1016/j.cosust.2011.08.001

    Article  Google Scholar 

  10. Vitousek PM, Naylor R, Crews T, David MB, Drinkwater LE, Holland E et al (2009) Nutrient imbalances in agricultural development. Science 324:1519–1520. doi:10.1126/science.1170261

    Article  CAS  PubMed  Google Scholar 

  11. Mendelsohn J, El Obeid S (2003) Sand and water. A profile of the Kavango region. Struik Publishers, Cape Town

    Google Scholar 

  12. Du R, Lu DR, Wang GC (2006) Diurnal, seasonal, and inter-annual variations of N2O fluxes from native semi-arid grassland soils of Inner Mongolia. Soil Biol Biochem 38:3474–3482. doi:10.1016/j.soilbio.2006.06.012

    Article  CAS  Google Scholar 

  13. Xu YQ, Wan SQ, Cheng WX, Li LH (2008) Impacts of grazing intensity on denitrification and N2O production in a semi-arid grassland ecosystem. Biogeochemistry 88:103–115. doi:10.1007/s10533-008-9197-4

    Article  CAS  Google Scholar 

  14. Weitz AM, Veldkamp E, Keller M, Neff J, Crill PM (1998) Nitrous oxide, nitric oxide, and methane fluxes from soils following clearing and burning of tropical secondary forest. J Geophys Res D: Atmos 103:28047–28058. doi:10.1029/98JD02144

    Article  CAS  Google Scholar 

  15. Stehfest E, Bouwman L (2006) N2O and NO emission from agricultural fields and soils under natural vegetation: summarizing available measurement data and modeling of global annual emissions. Nutr Cycl Agroecosyst 74:207–228. doi:10.1007/s10705-006-9000-7

    Article  CAS  Google Scholar 

  16. Conrad R (1996) Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiol Rev 60:609–640

    PubMed Central  CAS  PubMed  Google Scholar 

  17. McLain JET, Martens DA (2006) N2O production by heterotrophic N transformations in a semiarid soil. Appl Soil Ecol 32:253–263. doi:10.1016/j.apsoil.2005.06.005

    Article  Google Scholar 

  18. Peterjohn WT (1991) Denitrification: enzyme content and activity in desert soils. Soil Biol Biochem 23:845–855. doi:10.1016/0038-0717(91)90096-3

    Article  CAS  Google Scholar 

  19. Peterjohn WT, Schlesinger WH (1990) Nitrogen loss from deserts in the Southwestern United States. Biogeochemistry 10:67–79. doi:10.1007/BF00000893

    Article  Google Scholar 

  20. Jürgens N, Schmiedel U, Haarmeyer DH, Dengler J, Finckh M, Goetze D et al (2012) The BIOTA Biodiversity Observatories in Africa—a standardized framework for large-scale environmental monitoring. Environ Monit Assess 184:655–678. doi:10.1007/s10661-011-1993-y

    Article  PubMed  Google Scholar 

  21. Hartemink AE, Huting J (2008) Land cover, extent, and properties of arenosols in Southern Africa. Arid Land Res Manag 22:134–147. doi:10.1080/15324980801957689

    Article  CAS  Google Scholar 

  22. Klintenberg P, Seely M (2004) Land degradation monitoring in Namibia: a first approximation. Environ Monit Assess 99:5–21. doi:10.1007/s10661-004-3994-6

    Article  PubMed  Google Scholar 

  23. Haarmeyer DH, Luther-Mosebach J, Dengler J, Schmiedel U, Finckh M, Berger K et al. (2010) The BIOTA observatories. In: Jürgens N, Haarmeyer DH, Luther-Mosebach J, Dengler J, Finckh M, Schmiedel U (eds.): Biodiversity in southern Africa. Volume 1: patterns at local scale—the BIOTA Observatories, pp. 6–801, Klaus Hess Publishers, Göttingen & Windhoek.

  24. Gröngröft A, Herpel N, Petersen A, Mills A (2006) Indication of soil degradation processes in selected drylands of Southern Africa. Proceedings of the international conference: soil and desertification—integrated research for the sustainable management of soils in drylands. Hamburg, Germany

  25. Barnard P (1998) Biological diversity in Namibia—a country study. Namibian National Biodiversity Task Force, Windhoek

    Google Scholar 

  26. Uhlmann E, Görke C, Petersen A, Oberwinkler F (2004) Arbuscular mycorrhizae from semiarid regions of Namibia. Can J Bot 82:645–653. doi:10.1139/b04-039

    Article  CAS  Google Scholar 

  27. Strohbach BJ, Petersen A (2007) Vegetation of the central Kavango woodlands in Namibia: an example from the Mile 46 Livestock Development Centre. S Afr J Bot 73:391–401. doi:10.1016/j.sajb.2007.03.002

    Article  Google Scholar 

  28. Pröpper M, Gröngroft A, Falk T, Eschenbach A, Fox T, Gessner U et al. (2010) Causes and perspectives of land-cover change through expanding cultivation in Kavango. In: Biodiversity in southern Africa. Volume 3: implications for land use and management, pp. 1–31. Klaus Hess Publishers, Göttingen & Windhoek

  29. USDA (2002) Soil Survey Technical Note No. 2

  30. Wisch U, Petersen A, Gröngröft A, Eschenbach A (2009) Dryland farming in the Kavango region: effect of land use on soil properties. Zentralbl Geol Palaeontol Teil 1 2008:189–211

    Google Scholar 

  31. Smith MS, Tiedje JM (1979) Phases of denitrification following oxygen depletion in soil. Soil Biol Biochem 11:261–267. doi:10.1016/0038-0717(79)90071-3

    Article  CAS  Google Scholar 

  32. Yeates C, Gillings MR (1998) Rapid purification of DNA from soil for molecular biodiversity analysis. Lett Appl Microbiol 27:49–53. doi:10.1046/j.1472-765X.1998.00383.x

    Article  CAS  Google Scholar 

  33. Michotey V, Mejean V, Bonin P (2000) Comparison of methods for quantification of cytochrome cd 1-denitrifying bacteria in environmental marine samples. Appl Environ Microbiol 66:1564–1571. doi:10.1128/AEM.66.4.1564-1571.2000

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Throbäck IN, Enwall K, Jarvis Å, Hallin S (2004) Reassessing PCR primers targeting nirS, nirK and nosZ genes for community surveys of denitrifying bacteria with DGGE. FEMS Microbiol Ecol 49:401–417. doi:10.1016/j.femsec.2004.04.011

    Article  PubMed  Google Scholar 

  35. Braker G, Fesefeldt A, Witzel KP (1998) Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl Environ Microbiol 64:3769–3775

    PubMed Central  CAS  PubMed  Google Scholar 

  36. Braker G, Ayala-del-Rio HL, Devol AH, Fesefeldt A, Tiedje JM (2001) Community structure of denitrifiers, bacteria, and archaea along redox gradients in Pacific Northwest marine sediments by terminal restriction fragment length polymorphism analysis of amplified nitrite reductase (nirS) and 16S rRNA genes. Appl Environ Microbiol 67:1893–1901. doi:10.1128/AEM.67.4.1893-1901.2001

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. Dunbar J, Ticknor LO, Kuske CR (2001) Phylogenetic specificity and reproducibility and new method for analysis of terminal restriction fragment profiles of 16S rRNA genes from bacterial communities. Appl Environ Microbiol 67:190–197. doi:10.1128/AEM.67.1.190-197.2001

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Kandeler E, Deiglmayr K, Tscherko D, Bru D, Philippot L (2006) Abundance of narG, nirS, nirK, and nosZ genes of denitrifying bacteria during primary successions of a glacier foreland. Appl Environ Microbiol 72:5957–5962. doi:10.1128/AEM.00439-06

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd ed., XXVI, 488 p.

  40. Ter Braak CJF, Smilauer P (2002) Canoco reference manual and CanoDraw for Windows users guide: software for canonical community ordination [4.5]. Microcomputer Power, Ithaka

    Google Scholar 

  41. Nömmik H (1956) Investigations on denitrification in soil. Acta Agric Scand 6:195–228

    Article  Google Scholar 

  42. Zeidler J, Hanrahan S, Scholes M (2002) Land-use intensity affects range condition in arid to semi-arid Namibia. J Arid Environ 52:389–403. doi:10.1006/jare.2002.0990

    Article  Google Scholar 

  43. Burke IC, Lauenroth WK, Coffin DP (1995) Soil organic matter recovery in semiarid grasslands: implications for the conservation reserve program. Ecol Appl 5:793–801. doi:10.2307/1941987

    Article  Google Scholar 

  44. Enwall K, Throbäck IN, Stenberg M, Soderstrom M, Hallin S (2010) Soil resources influence spatial patterns of denitrifying communities at scales compatible with land management. Appl Environ Microbiol 76:2243–2250. doi:10.1128/AEM.02197-09

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Wu X, Liu G, Butterbach-Bahl K, Fu B, Zheng X, Brüggemann N (2013) Effects of land cover and soil properties on denitrification potential in soils of two semi-arid grasslands in Inner Mongolia, China. J Arid Environ 92:98–101

    Article  Google Scholar 

  47. Herrera-Arreola G, Vasquez-Murrieta MS, Cruz-Mondragon C, Van Cleemput O, Dendooven L (2008) Nitrous oxide emissions from soils of the semi-arid highlands of Durango, Mexico: a laboratory study. Arid Land Res Manag 22:179–194

    Article  CAS  Google Scholar 

  48. Frank DA, Groffman PM (1998) Denitrification in a semi-arid grazing ecosystem. Oecologia 117:564–569

    Article  Google Scholar 

  49. Scholes MC, Martin R, Scholes RJ, Parsons D, Winstead E (1997) NO and N2O emissions from savanna soils following the first simulated rains of the season. Nutr Cycl Agroecosyst 48:115–122. doi:10.1007/s004420050693

    Article  CAS  Google Scholar 

  50. Rees RM, Wuta M, Furley PA, Li C (2006) Nitrous oxide fluxes from savanna (miombo) woodlands in Zimbabwe. J Biogeogr 33:424–437. doi:10.1111/j.1365-2699.2005.01423.x

    Article  Google Scholar 

  51. Philippot L, Hallin S, Schloter M (2007) Ecology of denitrifying prokaryotes in agricultural soil. Adv Agron 96:249–305. doi:10.1016/S0065-2113(07)96003-4

    Article  CAS  Google Scholar 

  52. Tiedje JM (1988) Ecology of denitrification and of dissimilatory nitrate reduction to ammonium. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. John Wiley and Sons, Inc., New York, pp 179–244

    Google Scholar 

  53. Bossio DA, Girvan MS, Verchot L, Bullimore J, Borelli T, Albrecht A et al (2005) Soil microbial community response to land use change in an agricultural landscape of western Kenya. Microb Ecol 49:50–62. doi:10.1007/s00248-003-0209-6

    Article  CAS  PubMed  Google Scholar 

  54. Johnson CE, Johnson AH, Huntington TG, Siccama TG (1991) Whole-tree clear-cutting effects on soil horizons and organic-matter pools. Soil Sci Soc Am J 55:497–502. doi:10.2136/sssaj1991.03615995005500020034x

    Article  Google Scholar 

  55. Huygens D, Boeckx P, Van Cleemput O, Oyarzún C, Godoy R (2005) Aggregate and soil organic carbon dynamics in south Chilean andisols. Biogeosciences 2:159–174. doi:10.5194/bg-2-159-2005

    Article  CAS  Google Scholar 

  56. Bayer C, Martin-Neto L, Mielniczuk J, Pavinato A, Dieckow J (2006) Carbon sequestration in two Brazilian Cerrado soils under no-till. Soil Tillage Res 86:237–245. doi:10.1016/j.still.2005.02.023

    Article  Google Scholar 

  57. Christensen BT (2001) Physical fractionation of soil and structural and functional complexity in organic matter turnover. Eur J Soil Sci 52:345–353. doi:10.1046/j.1365-2389.2001.00417.x

    Article  CAS  Google Scholar 

  58. Abbadie L, Lensi R (1990) Carbon and nitrogen mineralization and denitrification in a humid savanna of West Africa (Côte d’Ivoire). Acta Oecol 11:717–728. doi:10.1029/95JD01923

    Google Scholar 

  59. Bremer C, Braker G, Matthies D, Beierkuhnlein C, Conrad R (2009) Plant presence and species combination, but not diversity, influence denitrifier activity and the composition of nirK-type denitrifier communities in grassland soil. FEMS Microbiol Ecol 70:377–387. doi:10.1111/j.1574-6941.2009.00732.x

    Article  CAS  PubMed  Google Scholar 

  60. Morales SE, Cosart T, Holben WE (2010) Bacterial gene abundances as indicators of greenhouse gas emission in soils. ISME J 4:799–808. doi:10.1038/ismej.2010.8

    Article  CAS  PubMed  Google Scholar 

  61. Cavigelli MA, Robertson GP (2000) The functional significance of denitrifier community composition in a terrestrial ecosystem. Ecology 81:1402–1414. doi:10.1890/0012-9658(2000)081%5B1402:TFSODC%5D2.0.CO;2

    Article  Google Scholar 

  62. Ka JO, Urbance J, Ye RW, Ahn TY, Tiedje JM (1997) Diversity of oxygen and N-oxide regulation of nitrite reductases in denitrifying bacteria. FEMS Microbiol Lett 156:55–60. doi:10.1111/j.1574-6968.1997.tb12705.x

    Article  CAS  PubMed  Google Scholar 

  63. Braker G, Dörsch P, Bakken LR (2012) Genetic characterization of denitrifier communities with contrasting intrinsic functional traits. FEMS Microbiol Ecol 79:542–554. doi:10.1111/j.1574-6941.2011.01237.x

    Article  CAS  PubMed  Google Scholar 

  64. Dries H, Pascal B, Pamela T, Leandro P, Oswald VC, Carlos ON et al (2008) Mechanisms for retention of bioavailable nitrogen in volcanic rainforest soils. Nat Geosci 1:543–548. doi:10.1038/ngeo252

    Article  Google Scholar 

  65. Muñoz C, Paulino L, Monreal C, Zagal E (2010) Greenhouse gas (CO2 and N2O) emissions from soils: a review. Chil J Agr Res 70:485–497

    Article  Google Scholar 

  66. Brümmer C, Brüggemann N, Butterbach-Bahl K, Falk U, Szarzynski J, Vielhauer K et al (2008) Soil-atmosphere exchange of N2O and NO in near-natural savanna and agricultural land in Burkina Faso (W. Africa). Biogeosciences 2008:582–600. doi:10.1007/s10021-008-9144-1

    Google Scholar 

  67. Castaldi S, Ariangelo DPR, John G, Nina N, Ruben M, José SJ (2004) Nitrous oxide and methane fluxes from soils of the Orinoco savanna under different land uses. Glob Chang Biol 10:1947–1960. doi:10.1111/j.1365-2486.2004.00871.x

    Article  Google Scholar 

  68. Dick J, Kaya B, Soutoura M, Skiba U, Smith R, Niang A, Tabo R (2008) The contribution of agricultural practices to nitrous oxide emissions in semi-arid Mali. Soil Use Manag 24:292–301. doi:10.1111/j.1475-2743.2008.00163.x

    Article  Google Scholar 

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Acknowledgments

This work was funded by the BIOTA South program of the German Federal Ministry of Education and Research (Project 01LC0621E/TP3) and the Max Planck Society.

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Correspondence to Gesche Braker.

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Braker, G., Matthies, D., Hannig, M. et al. Impact of Land Use Management and Soil Properties on Denitrifier Communities of Namibian Savannas. Microb Ecol 70, 981–992 (2015). https://doi.org/10.1007/s00248-015-0623-6

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