Bacterial community structure and microbial activity in different soils amended with biogas residues and cattle slurry
Abstract
Anaerobic digestion of organic materials generates residues of differing chemical composition compared to undigested animal manures, which may affect the soil microbial ecosystem differently when used as fertilizers. This study investigated the effects of two biogas residues (BR-A and BR-B) and cattle slurry (CS) applied at rates corresponding to 70kgNH4+-Nha−1 on bacterial community structure and microbial activity in three soils of different texture (a sandy, a clay and an organic clay soil). 16S rRNA genes were targeted in PCR reactions and bacterial community profiles visualized using terminal restriction fragment length polymorphism. General microbial activity was measured as basal respiration (B-resp), substrate-induced respiration (SIR), specific growth rate (μSIR), metabolic quotient (qCO2) and nitrogen mineralization capacity (NMC). Non-metric multidimensional scaling analysis visualized shifts in bacterial community structure related to microbial functions. There were significant differences in bacterial community structure after 120 days of incubation (+20°C at 70% of WHC) between non-amended (control) and amended soils, especially in the sandy soil, where CS caused a more pronounced shift than biogas residues. Terminal-restriction fragment (TRF) 307, the predominant peak in CS-amended sandy soil, was identified as possibly Bacillus or Streptococcus. TRF 226, the dominant peak in organic soil amended with BR-B, was classified as Rhodopseudomonas. B-resp significantly increased and SIR decreased in all amendments to organic soil compared with the control, potentially indicating decreased efficiency of heterotrophic microorganisms to convert organic carbon into microbial biomass. This was also reflected in an elevated qCO2 in the organic soil. The μSIR level was higher in the sandy soil amended with BR-A than with BR-B or CS, indicating a shift toward species capable of rapidly utilizing glucose. NMC was significantly elevated in the clay and organic soils amended with BR-A and BR-B and in the sandy soil amended with BR-B and CS. Thus, biogas residues and cattle slurry had different effects on the bacterial community structure and microbial activity in the three soils. However, the effects of biogas residues on microbial activities were comparable in magnitude to those of cattle slurry and the bacterial community structure was less affected. Therefore, we do not see any reason not to recommend using biogas residues as fertilizers based on the results presented.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Differences in soil microbial community and activity between manure and digestate were not such that they justified recommendation of either substrate before the other.
“While differences in soil microbial community and activity between manure and digestate were not such that they justified the recommendation of either substrate before the other (Abubaker et al., 2013), Insam et al. (2015) concluded that digestate could enhance soil microbial activity and biomass as compared to manure.”
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 Abubaker et al., 2013
Cites
16S ribosomal DNA amplification for phylogenetic study
Weisburg, W. G., Barns, S. M., Pelletier, D. A., & Lane, D. J. (1991) · Journal of Bacteriology · doi:10.1128/jb.173.2.697-703.1991 · Cited by 11,957 · see citing works
Methods of soil analysis. Part 3 - chemical methods.
Sparks, D. L., Page, A. L., Helmke, P. A., Loeppert, R. H., Soltanpour, P. N., Tabatabai, M. A., Johnston, C. T., & Sumner, M. E. (1996) · Cited by 8,502 · see citing works
The Varimax Criterion for Analytic Rotation in Factor Analysis
Kaiser, H. F. (1958) · Psychometrika · doi:10.1007/bf02289233 · Cited by 7,605 · see citing works
Scheffé, H. (1960) · Soil Science · doi:10.1097/00010694-196006000-00016 · Cited by 5,625 · see citing works
PC‐ORD: Multivariate Analysis of Ecological Data
(1998) · Bulletin of the Ecological Society of America · doi:10.2307/20168234 · Cited by 3,873 · see citing works
Methods in Applied Soil Microbiology and Biochemistry
(1995) · Elsevier eBooks · doi:10.1016/b978-0-12-513840-6.x5014-9 · Cited by 2,837 · see citing works
Biogas production: current state and perspectives
Weiland, P. (2009) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-009-2246-7 · Cited by 2,824 · see citing works
Biodiversity and ecosystem stability in a decade-long grassland experiment
Tilman, D. G., Reich, P. B., & Knops, J. M. H. (2006) · Nature · doi:10.1038/nature04742 · Cited by 2,310 · see citing works
Multivariate Analysis of Ecological Data
Lepš, J., & Šmilauer, P. (2006) · Bulletin of the Ecological Society of America · doi:10.1890/0012-9623(2006)87[193:maoed]2.0.co;2 · Cited by 2,080 · see citing works
Lauber, C. L., Strickland, M. S., Bradford, M. A., & Fierer, N. (2008) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2008.05.021 · Cited by 1,829 · see citing works
Mulvaney, R. L. (1996) · Soil Science Society of America book series · doi:10.2136/sssabookser5.3.c38 · Cited by 1,730 · see citing works
A Primer of Ecological Statistics
Ford, E. D. (2005) · The American Statistician · doi:10.1198/tas.2005.s32 · Cited by 1,551 · see citing works
Principles and Applications of Soil Microbiology
Gentry, T. J., Fuhrmann, J. J., & Zuberer, D. A. (2021) · Elsevier eBooks · doi:10.1016/c2018-0-05260-3 · Cited by 1,378 · see citing works
Demirel, B., & Scherer, P. (2008) · Reviews in Environmental Science and Bio/Technology · doi:10.1007/s11157-008-9131-1 · Cited by 1,200 · see citing works
Gerard Muyzer, C., Teske, A., Wirsen, C. O., & Jannasch, H. W. (1995) · Archives of Microbiology · doi:10.1007/bf02529967 · Cited by 1,112 · see citing works
Anaerobic digestion in global bio-energy production: Potential and research challenges
Appels, L., Lauwers, J., Degrève, J., Helsen, L., Lievens, B., Willems, K., van Impe, J. F. M., & Dewil, R. (2011) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2011.07.121 · Cited by 959 · see citing works
Biogas from Waste and Renewable Resources
(2008) · Wiley eBooks · doi:10.1002/9783527621705 · Cited by 855 · see citing works
Girvan, M. S., Bullimore, J., Pretty, J., Osborn, A. M., & Ball, A. S. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.3.1800-1809.2003 · Cited by 811 · see citing works
Kowalchuk, G. A., Stephen, J. R., de Boer, W., et al. (1997) · Applied and Environmental Microbiology · doi:10.1128/aem.63.4.1489-1497.1997 · Cited by 804 · see citing works
Wardle, D. A., & Ghani, A. (1995) · Soil Biology and Biochemistry · doi:10.1016/0038-0717(95)00093-t · Cited by 779 · see citing works
Soil microbial diversity and the sustainability of agricultural soils
Kennedy, A. C., & Smith, K. L. (1995) · Plant and Soil · doi:10.1007/bf02183056 · Cited by 745 · see citing works
Ammonium Production in Soil under Waterlogged Conditions as an Index of Nitrogen Availability
WARING, S. A., & Bremner, J. M. (1964) · Nature · doi:10.1038/201951a0 · Cited by 638 · see citing works
Relationships between soil pH and microbial properties in a UK arable soil
Pietri, J. C. A., & Brookes, P. C. (2008) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2008.03.020 · Cited by 592 · see citing works
Nacke, H., Thürmer, A., Wollherr, A., Will, C., Hodač, L., Herold, N., Schöning, I., Schrumpf, M., & Daniel, R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017000 · Cited by 560 · see citing works
Relationships of soil respiration to microbial biomass, substrate availability and clay content
Wang, W., Dalal, R. C., Moody, P. W., & Smith, C. J. (2003) · Soil Biology and Biochemistry · doi:10.1016/s0038-0717(02)00274-2 · Cited by 522 · see citing works
Soil microbial community responses to dairy manure or ammonium nitrate applications
Peacock, A. D., Mullen, M. D., Ringelberg, D. B., Tyler, D. D., Hedrick, D. B., Gale, P. M., & White, D. C. (2001) · Soil Biology and Biochemistry · doi:10.1016/s0038-0717(01)00004-9 · Cited by 451 · see citing works
McCaig, A. E., Glover, L. A., & Prosser, J. I. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.4.1721-1730.1999 · Cited by 439 · see citing works
Enwall, K., Philippot, L., & Hallin, S. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.12.8335-8343.2005 · Cited by 359 · see citing works
van Diepeningen, A. D., de Vos, O. J., Korthals, G. W., & van Bruggen, A. H. C. (2005) · Applied Soil Ecology · doi:10.1016/j.apsoil.2005.03.003 · Cited by 345 · see citing works
Weintraub, M., & Schimel, J. (2002) · Ecosystems · doi:10.1007/s10021-002-0124-6 · Cited by 325 · see citing works
Soil microbial biomass—what do the numbers really mean?
Dalal, R. C. (1998) · Australian Journal of Experimental Agriculture · doi:10.1071/ea97142 · Cited by 310 · see citing works
Logsdon, S. D. (2008) · Soil Science Society of America Journal · doi:10.2136/sssaj2008.0003br · Cited by 293 · see citing works
Biogas residues as fertilisers – Effects on wheat growth and soil microbial activities
Abubaker, J., Risberg, K., & Pell, M. (2012) · Applied Energy · doi:10.1016/j.apenergy.2012.04.050 · Cited by 258 · see citing works
Self-citationMicrobial biomass and activities in soil as affected by frozen and cold storage
Stenberg, B., Johansson, M., Pell, M., Svensson, K., Stenström, J., & Torstensson, L. (1998) · Soil Biology and Biochemistry · doi:10.1016/s0038-0717(97)00125-9 · Cited by 250 · see citing works
Self-citationvan Beelen, P., & Doelman, P. (1997) · Chemosphere · doi:10.1016/s0045-6535(96)00388-8 · Cited by 250 · see citing works
Shyu, C., Soule, T., Bent, S. J., et al. (2007) · Microbial Ecology · doi:10.1007/s00248-006-9106-0 · Cited by 241 · see citing works
Soil and plant effects on microbial community structure
Buyer, J. S., Roberts, D. P., & Russek‐Cohen, E. (2002) · Canadian Journal of Microbiology · doi:10.1139/w02-095 · Cited by 218 · see citing works
Land application of organic waste – Effects on the soil ecosystem
Odlare, M., Arthurson, V., Pell, M., Svensson, K., Nehrenheim, E., & Abubaker, J. (2011) · Applied Energy · doi:10.1016/j.apenergy.2010.12.043 · Cited by 208 · see citing works
Self-citationMöller, K., Stinner, W., Deuker, A., & Leithold, G. (2008) · Nutrient Cycling in Agroecosystems · doi:10.1007/s10705-008-9196-9 · Cited by 204 · see citing works
Improved Detection of Bifidobacteria with Optimised 16S rRNA-Gene Based Pyrosequencing
Sim, K., Cox, M. J., Wopereis, H., Martı́n, R., Knol, J., Li, M., Cookson, W., Moffatt, M. F., & Kroll, J. S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032543 · Cited by 196 · see citing works
Soil sampling, handling, storage and analysis
Forster, J. C. (1995) · Elsevier eBooks · doi:10.1016/b978-012513840-6/50018-5 · Cited by 176 · see citing works
Composition of fresh, aerobic and anaerobic farm animal dungs
Kirchmann, H., & Witter, E. (1992) · Bioresource Technology · doi:10.1016/0960-8524(92)90199-8 · Cited by 173 · see citing works
Soil science: Sustainable production and environmental protection
Mckeague, A. (1997) · Geoderma · doi:10.1016/s0016-7061(97)00067-0 · Cited by 165 · see citing works
Developments in soil microbiology since the mid 1960s
Insam, H. (2001) · Geoderma · doi:10.1016/s0016-7061(01)00029-5 · Cited by 151 · see citing works
Reversible transition between active and dormant microbial states in soil
Stenström, J., Svensson, K., & Johansson, M. (2001) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2001.tb00829.x · Cited by 146 · see citing works
Goberna, M., Podmirseg, S. M., Waldhuber, S., Knapp, B. A., García, C., & Insam, H. (2011) · Applied Soil Ecology · doi:10.1016/j.apsoil.2011.07.007 · Cited by 138 · see citing works
Chen, R., Blagodatskaya, E., Senbayram, M., Blagodatsky, S., Myachina, O., Dittert, K., & Kuzyakov, Y. (2012) · Biomass and Bioenergy · doi:10.1016/j.biombioe.2012.06.014 · Cited by 127 · see citing works
Parham, J. A., Deng, S. P., Da, H. N., et al. (2003) · Biology and Fertility of Soils · doi:10.1007/s00374-003-0657-7 · Cited by 127 · see citing works
Govasmark, E., Stäb, J., Holen, B., Hoornstra, D., Nesbakk, T., & Salkinoja-Salonen, M. (2011) · Waste Management · doi:10.1016/j.wasman.2011.07.025 · Cited by 125 · see citing works
A method for determining microbially available N and P in an organic soil
Nordgren, A. (1992) · Biology and Fertility of Soils · doi:10.1007/bf00340575 · Cited by 110 · see citing works
Hankinson, T. R., & Schmidt, E. L. (1988) · Applied and Environmental Microbiology · doi:10.1128/aem.54.6.1536-1540.1988 · Cited by 107 · see citing works
Carbon and Nitrogen Dynamics During Incubation of Manured Soil
Calderón, F. J., McCarty, G. W., Kessel, J. A. S. V., et al. (2004) · Soil Science Society of America Journal · doi:10.2136/sssaj2004.1592 · Cited by 102 · see citing works
Reversible transition between active and dormant microbial states in soil
Stenström, J. (2001) · FEMS Microbiology Ecology · doi:10.1016/s0168-6496(01)00122-2 · Cited by 99 · see citing works
The interaction between aluminium and root nodule bacteria
Flis, S. E., Glenn, A. R., & DILWORTH, M. J. (1993) · Soil Biology and Biochemistry · doi:10.1016/0038-0717(93)90066-k · Cited by 97 · see citing works
Wang, W., Chalk, P. M., Chen, D., et al. (2001) · Soil Biology and Biochemistry · doi:10.1016/s0038-0717(01)00034-7 · Cited by 89 · see citing works
Residues from renewable energy production: Their value for fertilizing pastures
Bougnom, B. P., Niederkofler, C., Knapp, B. A., Stimpfl, E., & Insam, H. (2012) · Biomass and Bioenergy · doi:10.1016/j.biombioe.2012.01.017 · Cited by 84 · see citing works
Ozores-Hampton, M., Stansly, P. A., & Salamé, T. P. (2011) · Journal of Sustainable Agriculture · doi:10.1080/10440046.2011.554289 · Cited by 83 · see citing works
Larkin, R. P., Honeycutt, C. W., & Griffin, T. S. (2005) · Biology and Fertility of Soils · doi:10.1007/s00374-005-0060-7 · Cited by 83 · see citing works
The close phylogenetic relationship of Nitrobacter and Rhodopseudomonas palustris
Seewaldt, E., Schleifer, K., Bock, E., et al. (1982) · Archives of Microbiology · doi:10.1007/bf00405895 · Cited by 75 · see citing works
Bagge, E., Persson, M., & Johansson, K.-E. (2010) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2010.04790.x · Cited by 70 · see citing works
Fertilizer Recovery from Anaerobic Digesters
Field, J. A., Caldwell, J. S., Jeyanayagam, S., Reneau, R. B., Jr., Kroontje, W., Collins, E., & Jr. (1984) · Transactions of the ASAE · doi:10.13031/2013.33060 · Cited by 64 · see citing works
SOIL CARBON DYNAMICS DURING A LONG-TERM INCUBATION STUDY INVOLVING 13C AND 14C MEASUREMENTS
Follett, R. F., Paul, E. A., & Pruessner, E. G. (2007) · Soil Science · doi:10.1097/ss.0b013e31803403de · Cited by 56 · see citing works
Degradation of furfural (2- furaldehyde) to methane and carbon dioxide by an anaerobic consortium
Rivard, C. J., & Grohmann, K. (1991) · Applied Biochemistry and Biotechnology · doi:10.1007/bf02922608 · Cited by 50 · see citing works
Zhang, D., Yang, H., Huang, Z., et al. (2002) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/00207713-52-6-2055 · Cited by 42 · see citing works
Sawada, K., Funakawa, S., & Kosaki, T. (2009) · Soil Science & Plant Nutrition · doi:10.1111/j.1747-0765.2009.00378.x · Cited by 21 · see citing works
Wu, F.-S. (2012) · African Journal of Microbiology Research · doi:10.5897/ajmr12.562 · Cited by 17 · see citing works
Zhang, D. (2002) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.02259-0 · Cited by 16 · see citing works
Burke, M. E., Gorham, E., & Pratt, D. C. (1974) · Journal of Bacteriology · doi:10.1128/jb.117.2.826-833.1974 · Cited by 14 · see citing works
Dalapicolla, J., do Prado, J. R., Percequillo, A. R., & Knowles, L. L. (2021) · Journal of Biogeography · doi:10.1111/jbi.14281 · Cited by 12 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Manure-based biogas fermentation residues – friend or foe of soil fertility?
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
Schröder, 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
- Authors
- Abubaker, J., Cederlund, H., Arthurson, V., & Pell, M.
- Affiliations
- Swedish University of Agricultural Sciences (SE)
- Corresponding author
- Abubaker, J.
- Venue
- Applied Soil Ecology
- Publisher
- Elsevier BV
- Published
- 2013-10
- Volume
- 72
- Pages
- 171-180
- ISSN
- 0929-1393 (ISSN-L)
- OpenAlex
- W2061166993
- Cited by
- 98
- References
- 71
- Citations by year
- 2026: 6 · 2025: 10 · 2024: 7 · 2023: 7 · 2022: 5 · 2021: 14 · 2020: 8 · 2019: 9 · 2018: 7 · 2017: 7 · 2016: 5 · 2015: 10 · 2014: 3
- FWCI
- 8.69
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Applied Soil Ecology (publishedVersion)
- Funders
- Sveriges Lantbruksuniversitet
- Topics
- Life Sciences › Agricultural and Biological Sciences › Soil Science › Soil Carbon and Nitrogen Dynamics
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Life Sciences › Agricultural and Biological Sciences › Soil Science › Agricultural Science and Fertilization
- Keywords
- biogas residue, cattle slurry, soil bacterial community structure, microbial activity, soil amendment, nitrogen mineralization, basal respiration, substrate-induced respiration, metabolic quotient, soil texture, 16S rRNA gene, Rhodopseudomonas, Bacillus, Streptococcus, organic fertilizer
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review