Pathogenic bacteria and mineral N in soils following the land spreading of biogas digestates and fresh manure
Abstract
The on-farm production of renewable energy from animal manures has rapidly expanded in central and northern Europe, with thousands of anaerobic reactors. This process has increased the land spreading of biogas digestates, replacing the use of fresh manure as a fertiliser. The environmental benefits and risks of such a change still need to be defined. We hypothesised that applying to the soil anaerobically digested instead of fresh manure might control the release of pathogens but increase that of inorganic N. Pots including γ- or non-irradiated soils, either control or amended with digestate or manure (80kgNhaâ»Â¹), were incubated for 0, 1 and 3 months. Escherichia coli, Salmonella and Listeria were cultivated and pathogenicity genes invA and hlyA PCR-amplified. Soil ammonium and nitrate concentrations, and their leaching through the upper soil layer was quantified in 20cm-depth lysimeters for 100d. Anaerobic digestion significantly sanitised the manure by completely eliminating cultivable E. coli and Salmonella but not Listeria (1.7Ã10â´CFUsgâ»Â¹). Thus, manure increased all microbes and invA gene numbers when applied to soils, while the digestate supplied only hlyA-negative Listeria. Potential pathogens were significantly more abundant in γ- than in non-irradiated treatments indicating suppression by indigenous soil microbiota. Control levels of all potential pathogens were recovered after 3 months, which could be thus considered a safe delay between land spreading amendments and harvesting. Concentration of nitrates in soil and their movement through the upper layer in soils amended with digestate were doubled compared to the other treatments. Hence, care should be taken that in the field nitrate liberation does not exceed plant demand.
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Concentration of nitrate in upper soil layers is higher after application of digestate than after manure application.
“Moreover, experimental studies show that the concentration of nitrate in upper soil layers is higher after application of digestate than after manure application (Goberna et al., 2011).”
From Intensify production, transform biomass to energy and novel goods and protect soils in Europe—A vision how to mobilize marginal lands (2018) · cites this paper as Goberna et al., 2011
Cites
Biological control of soil-borne pathogens by fluorescent pseudomonads
Haas, D., & Défago, G. (2005) · Nature Reviews Microbiology · doi:10.1038/nrmicro1129 · Cited by 2,611 · see citing works
The future of anaerobic digestion and biogas utilization
Holm‐Nielsen, J. B., Seadi, T. A., & Oleśkowicz-Popiel, P. (2009) · Bioresource Technology · doi:10.1016/j.biortech.2008.12.046 · Cited by 1,620 · see citing works
Phases of denitrification following oxygen depletion in soil
Smith, M. S., & Tiedje, J. M. (1979) · Soil Biology and Biochemistry · doi:10.1016/0038-0717(79)90071-3 · Cited by 745 · see citing works
Ammonia emission from field applied manure and its reduction—invited paper
Sommer, S. G., & Hutchings, N. J. (2001) · European Journal of Agronomy · doi:10.1016/s1161-0301(01)00112-5 · Cited by 602 · see citing works
Pathogen survival during livestock manure storage and following land application
Nicholson, F. A., Groves, S. J., & CHAMBERS, B. J. (2004) · Bioresource Technology · doi:10.1016/j.biortech.2004.02.030 · Cited by 508 · see citing works
Birkett, J., & Lester, J. (2010) · Taylor & Francis eBooks · doi:10.4324/9780203477397_chapter_18 · Cited by 434 · see citing works
Sterilization and inhibition of microbial activity in soil
Trevors, J. T. (1996) · Journal of Microbiological Methods · doi:10.1016/0167-7012(96)00843-3 · Cited by 409 · see citing works
A review of survival of pathogenic bacteria in organic waste used in biogas plants
Sahlström, L. M. O. (2002) · Bioresource Technology · doi:10.1016/s0960-8524(02)00168-2 · Cited by 393 · see citing works
Berns, A. E., Philipp, H., Narres, H. D., et al. (2008) · European Journal of Soil Science · doi:10.1111/j.1365-2389.2008.01016.x · Cited by 361 · see citing works
Pathogens in livestock waste, their potential for movement through soil and environmental pollution
Mawdsley, J. L., Bardgett, R. D., Merry, R. J., et al. (1995) · Applied Soil Ecology · doi:10.1016/0929-1393(94)00039-a · Cited by 293 · see citing works
Möller, K., & Stinner, W. (2008) · European Journal of Agronomy · doi:10.1016/j.eja.2008.06.003 · Cited by 270 · see citing works
Nitrogen in biowaste and yard waste compost: dynamics of mobilisation and availability—a review
Amlinger, F., Götz, B., Dreher, P., Geszti, J., & Weissteiner, C. J. (2003) · European Journal of Soil Biology · doi:10.1016/s1164-5563(03)00026-8 · Cited by 266 · see citing works
Nogva, H. K., Rudi, K., Naterstad, K., et al. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.10.4266-4271.2000 · Cited by 255 · see citing works
Transport of bacteria from manure and protection of water resources
Unc, A., & Goss, M. J. (2003) · Applied Soil Ecology · doi:10.1016/j.apsoil.2003.08.007 · Cited by 245 · see citing works
The role of indigenous microorganisms in suppression of salmonella regrowth in composted biosolids
Sidhu, J. P. S. (2001) · Water Research · doi:10.1016/s0043-1354(00)00352-3 · Cited by 200 · see citing works
Bodenbiologische Arbeitsmethoden
(1993) · Springer eBooks · doi:10.1007/978-3-642-77936-7 · Cited by 186 · see citing works
Bacterial pathogen incidences in sludge from Swedish sewage treatment plants
Sahlström, L. M. O., Aspán, A., Bagge, E., Danielsson‐Tham, M., & Albihn, A. (2004) · Water Research · doi:10.1016/j.watres.2004.01.031 · Cited by 172 · see citing works
Venglovský, J., Sasáková, N., & Plachá, I. (2009) · Bioresource Technology · doi:10.1016/j.biortech.2009.03.068 · Cited by 170 · see citing works
Snell‐Castro, R., Godon, J., ̈s, J.-P. D., & Dabert, P. (2004) · FEMS Microbiology Ecology · doi:10.1016/j.femsec.2004.11.016 · Cited by 164 · see citing works
Teglia, C., Trémier, A., & Martel, J.-L. (2010) · Waste and Biomass Valorization · doi:10.1007/s12649-010-9051-5 · Cited by 161 · see citing works
The effect of hygienic treatment on the microbial flora of biowaste at biogas plants
Bagge, E., Sahlström, L. M. O., & Albihn, A. (2005) · Water Research · doi:10.1016/j.watres.2005.03.016 · Cited by 143 · see citing works
Microbes at work: from wastes to resources
(2010) · Choice Reviews Online · doi:10.5860/choice.48-0250 · Cited by 127 · see citing works
Bacterial decimation times in anaerobic digestions of animal slurries
Olsen, J. E., & Larsen, H. E. (1987) · Biological Wastes · doi:10.1016/0269-7483(87)90121-2 · Cited by 123 · see citing works
Terhoeven‐Urselmans, T., Scheller, E., Raubuch, M., Ludwig, B., & Joergensen, R. G. (2009) · Applied Soil Ecology · doi:10.1016/j.apsoil.2009.05.012 · Cited by 116 · see citing works
Sandars, D. L., Audsley, E., Cañete, C. M. R., Cumby, T. R., Scotford, I. M., & Williams, A. G. (2003) · Biosystems Engineering · doi:10.1016/s1537-5110(02)00278-7 · Cited by 114 · see citing works
Goberna, M., Insam, H., & Franke‐Whittle, I. H. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.02260-08 · Cited by 112 · see citing works
Self-citationGirardin, H., Morris, C. E., Albagnac, C., et al. (2005) · FEMS Microbiology Ecology · doi:10.1016/j.femsec.2005.04.003 · Cited by 110 · see citing works
Survival of pathogenic bacteria during mesophilic anaerobic digestion of animal waste
Kearney, T. E., Larkin, M. J., Frost, J. P., et al. (1993) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1993.tb02768.x · Cited by 109 · see citing works
Zaleski, K. J., Josephson, K. L., Gerba, C. P., et al. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.7.3701-3708.2005 · Cited by 101 · see citing works
Occurrence, growth, and suppression of salmonellae in composted sewage sludge
Hussong, D., Burge, W. D., & Enkiri, N. K. (1985) · Applied and Environmental Microbiology · doi:10.1128/aem.50.4.887-893.1985 · Cited by 92 · see citing works
Insam, H., Franke-Whittle, I., & Goberna, M. (2009) · Springer eBooks · doi:10.1007/978-3-642-04043-6 · Cited by 91 · see citing works
Self-citationSurvival of Bacillus thuringiensis Spores in Soil
Petras, S. F., & Casida, L. E. (1985) · Applied and Environmental Microbiology · doi:10.1128/aem.50.6.1496-1501.1985 · Cited by 88 · see citing works
Pepper, I. L., Brooks, J. P., & Gerba, C. P. (2006) · Advances in agronomy · doi:10.1016/s0065-2113(06)90001-7 · Cited by 86 · see citing works
Nitrogen mobility in a nitrogen limited forest at Klosterhede, Denmark, examined by NH4NO3 addition
Gundersen, P., & Rasmussen, L. (1995) · Forest Ecology and Management · doi:10.1016/0378-1127(94)06085-w · Cited by 85 · see citing works
Microbial competition: effect of Pseudomonas fluorescens on the growth of Listeria monocytogenes
Buchanan, R. L., & Bagi, L. K. (1999) · Food Microbiology · doi:10.1006/fmic.1998.0264 · Cited by 85 · see citing works
Gamma Radiation Compared with Steam and Methyl Bromide as a Soil Sterilizing Agent
Eno, C. F., & Popenoe, H. (1964) · Soil Science Society of America Journal · doi:10.2136/sssaj1964.03615995002800040024x · Cited by 76 · see citing works
Microbes in Aerobic and Anaerobic Waste Treatment
Insam, H., Franke‐Whittle, I. H., & Goberna, M. (2009) · Springer eBooks · doi:10.1007/978-3-642-04043-6_1 · Cited by 73 · see citing works
Self-citationSimultaneous detection of Salmonella spp and Escherichia coli O157:H7 by multiplex PCR
Fratamico, P. M., & Strobaugh, T. P. (1998) · Journal of Industrial Microbiology & Biotechnology · doi:10.1038/sj.jim.2900520 · Cited by 66 · see citing works
NITROGEN LEACHING FROM FOREST SOIL CORES AFTER AMENDING ORGANIC RECYCLING PRODUCTS AND FERTILIZERS
Insam, H. (1997) · Waste Management & Research The Journal for a Sustainable Circular Economy · doi:10.1006/wmre.1996.0084 · Cited by 57 · see citing works
Self-citationNitrogen Leaching From Forest Soil Cores After Amending Organic Recycling Products and Fertilizers
Insam, H., & Merschak, P. (1997) · Waste Management & Research The Journal for a Sustainable Circular Economy · doi:10.1177/0734242x9701500306 · Cited by 51 · see citing works
Self-citationIdentification of Listeria innocua by PCR targeting a putative transcriptional regulator gene
Liu, D., Ainsworth, A. J., Austin, F. W., et al. (2003) · FEMS Microbiology Letters · doi:10.1016/s0378-1097(03)00378-1 · Cited by 50 · see citing works
Matsunaka, T., Sawamoto, T., Ishimura, H., Takakura, K., & Takekawa, A. (2006) · International Congress Series · doi:10.1016/j.ics.2006.03.016 · Cited by 49 · see citing works
Ottoson, J., Schnürer, A., & Vinnerås, B. (2008) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2007.02317.x · Cited by 47 · see citing works
Vinnerås, B., Schönning, C., & Nordin, A. (2006) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2006.02.008 · Cited by 31 · see citing works
Anaerobic Digestion of Agricultural Residues
O’Flaherty, V., Collins, G., & Mahony, T. (2009) · Environmental Microbiology · doi:10.1002/9780470495117.ch11 · Cited by 18 · see citing works
Lim, S.-S., Kwak, J., Lee, S.-I., et al. (2010) · Journal of Soils and Sediments · doi:10.1007/s11368-010-0263-x · Cited by 16 · see citing works
Miller, J. J., Beasley, B. W., Chanasyk, D. S., et al. (2008) · Compost Science & Utilization · doi:10.1080/1065657x.2008.10702350 · Cited by 12 · see citing works
Biogas Technology – Controlled Gas Flow for Enhanced Mixing, Heating, and Desulfurization
Wett, B., & Insam, H. (2009) · Springer eBooks · doi:10.1007/978-3-642-04043-6_4 · Cited by 9 · see citing works
Self-citationEffects of digestate on the environment and on plant production - results of a research project
Fuchs, J. G., Baier, U., Berner, A., et al. (2008) · Organic Eprints (International Centre for Research in Organic Food Systems, and Research Institute of Organic Agriculture) · Cited by 3 · see citing works
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Insam, H., Gómez-Brandón, M., & Ascher, J. (2015) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2015.02.006 · Cited by 321 · see citing works
Self-citationKlammsteiner, T., Turan, V., Fernández-Delgado Juárez, M., Oberegger, S., & Insam, H. (2020) · Agronomy · doi:10.3390/agronomy10101578 · Cited by 223 · see citing works
Self-citationSchröder, P., Beckers, B., Daniels, S., Gnädinger, F., Maestri, E., Marmiroli, N., Mench, M., Millan, R., Obermeier, M. M., Oustriere, N., et al. (2018) · Science of The Total Environment · doi:10.1016/j.scitotenv.2017.10.209 · Cited by 151 · see citing works
Abubaker, J., Cederlund, H., Arthurson, V., & Pell, M. (2013) · Applied Soil Ecology · doi:10.1016/j.apsoil.2013.07.002 · Cited by 98 · see citing works
Demirel, B., Göl, N. P., & Onay, T. T. (2013) · Journal of Material Cycles and Waste Management · doi:10.1007/s10163-012-0107-4 · Cited by 61 · see citing works
- Authors
- Goberna, M., Podmirseg, S. M., Waldhuber, S., Knapp, B. A., García, C., & Insam, H.
- Affiliations
- Universität Innsbruck (AT)
- Centro de Edafología y Biología Aplicada del Segura (ES)
- Corresponding author
- Goberna, M.
- Venue
- Applied Soil Ecology
- Publisher
- Elsevier BV
- Published
- 2011-09
- Volume
- 49
- Pages
- 18-25
- ISSN
- 0929-1393 (ISSN-L)
- OpenAlex
- W2067761513
- Cited by
- 138
- References
- 49
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 10 · 2023: 9 · 2022: 12 · 2021: 8 · 2020: 16 · 2019: 12 · 2018: 9 · 2017: 9 · 2016: 9 · 2015: 12 · 2014: 7 · 2013: 14 · 2012: 5
- FWCI
- 8.07
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Applied Soil Ecology (publishedVersion)
- Topics
- Physical Sciences › Environmental Science › Water Science and Technology › Fecal contamination and water quality
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Listeria monocytogenes in Food Safety
- Life Sciences › Agricultural and Biological Sciences › Soil Science › Soil Carbon and Nitrogen Dynamics
- Keywords
- biogas digestate, fresh manure, anaerobic digestion, soil-borne pathogens, Escherichia coli, Salmonella, Listeria, inorganic nitrogen, nitrate leaching, ammonium, gamma irradiation, soil microbiota, pathogen inhibition, land spreading
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