Microbial indicators for soil quality
Open accessAbstract
The living soil is instrumental to key life support functions (LSF) that safeguard life on Earth. The soil microbiome has a main role as a driver of these LSF. Current global developments, like anthropogenic threats to soil (e.g., via intensive agriculture) and climate change, pose a burden on soil functioning. Therefore, it is important to dispose of robust indicators that report on the nature of deleterious changes and thus soil quality. There has been a long debate on the best selection of biological indicators (bioindicators) that report on soil quality. Such indicators should ideally describe organisms with key functions in the system, or with key regulatory/connecting roles (so-called keystone species ). However, in the light of the huge functional redundancy in most soil microbiomes, finding specific keystone markers is not a trivial task. The current rapid development of molecular (DNA-based) methods that facilitate deciphering microbiomes with respect to key functions will enable the development of improved criteria by which molecular information can be tuned to yield molecular markers of soil LSF. This review critically examines the current state-of-the-art in molecular marker development and recommends avenues to come to improved future marker systems.
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A large proportion of soil organisms remains to be characterized in taxonomic and functional terms.
“since a large proportion of soil organisms yet remains to be characterized in taxonomic and functional terms (Schloter et al., 2018; Bouchez et al., 2016).”
From Soil quality – A critical review (2018) · cites this paper as Schloter et al., 2018
In “The soil microbiome—an ignored majority” (page unavailable), the paper says that efforts to characterize the soil microbiome in depth have been hindered by its complexity. In “Soil microbiome functions that drive nitrogen transformations” (page unavailable), it also says that knowledge of some organisms and their genes is lacking. These passages support the point for soil microorganisms, but not its extension to soil organisms generally. (LLM, conf=0.80)
Experimental — accuracy not yet measuredThe analysis of the 'big data' generated with sequencing poses a serious challenge in terms of time, computing capacities and interpretation.
“The analysis of the ' big data ' generated with sequencing also poses a serious challenge in terms of time, computing capacities and interpretation”
From Soil quality – A critical review (2018) · cites this paper as Schloter et al., 2018
In “The soil microbiome—an ignored majority” (page not provided), the paper says sequencing generates “big data” that challenge bioinformatics analysis. “Brave new world” also notes interpretational pitfalls for high-throughput sequencing. The cited passages do not specify analysis time or computing-capacity demands; their reference to time concerns sampling, not data analysis. (LLM, conf=0.88)
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Cites
The rhizosphere microbiome and plant health
Berendsen, R. L., Pieterse, C. M. J., & Bakker, P. A. H. M. (2012) · Trends in Plant Science · doi:10.1016/j.tplants.2012.04.001 · Cited by 5,347 · see citing works
Escherichia coli and Salmonella typhimurium: Cellular and molecular biology
Lejeune, P. (1988) · Biochimie · doi:10.1016/0300-9084(88)90119-8 · Cited by 4,086 · see citing works
Lauber, C. L., Hamady, M., Knight, R., & Fierer, N. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.00335-09 · Cited by 4,063 · see citing works
Using network analysis to explore co-occurrence patterns in soil microbial communities
Barberán, A., Bates, S. T., Casamayor, E. O., & Fierer, N. (2012) · The ISME Journal · doi:10.1038/ismej.2011.119 · Cited by 3,044 · see citing works
Defining Soil Quality for a Sustainable Environment
(1994) · SSSA special publication series · doi:10.2136/sssaspecpub35 · Cited by 2,193 · see citing works
Defining and Assessing Soil Quality
Doran, J. W., & Parkin, T. B. (1994) · SSSA Special Publications · doi:10.2136/sssaspecpub35.c1 · Cited by 2,176 · see citing works
Muyzer, G., & Smalla, K. (1998) · Antonie van Leeuwenhoek · doi:10.1023/a:1000669317571 · Cited by 2,051 · see citing works
Microbial diversity and soil functions
Nannipieri, P., Ascher‐Jenull, J., Ceccherini, M. T., Landi, L., Pietramellara, G., & Renella, G. (2003) · European Journal of Soil Science · doi:10.1046/j.1351-0754.2003.0556.x · Cited by 1,863 · see citing works
Self-citationMicrobial diversity and soil functions
Nannipieri, P., Ascher‐Jenull, J., Ceccherini, M. T., Landi, L., Pietramellara, G., & Renella, G. (2017) · European Journal of Soil Science · doi:10.1111/ejss.4_12398 · Cited by 1,733 · see citing works
Self-citationStaley, J. T., & Konopka, A. E. (1985) · Annual Review of Microbiology · doi:10.1146/annurev.mi.39.100185.001541 · Cited by 1,512 · see citing works
Burris, R. H., & Roberts, G. P. (1993) · Annual Review of Nutrition · doi:10.1146/annurev.nu.13.070193.001533 · Cited by 1,464 · see citing works
The Soil Management Assessment Framework: A Quantitative Soil Quality Evaluation Method
Andrews, S. S., Karlen, D. L., & Cambardella, C. A. (2004) · Soil Science Society of America Journal · doi:10.2136/sssaj2004.1945 · Cited by 1,341 · cited 1× · see citing works
“For example, of the ten indicators used to evaluate soil quality given by Andrews et al. (2004), only two (microbial biomass C and potential N mineralization) address microbiological soil properties.”
BackgroundActive microorganisms in soil: Critical review of estimation criteria and approaches
Blagodatskaya, E. V., & Kuzyakov, Y. V. (2013) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2013.08.024 · Cited by 1,059 · see citing works
Lipsewers, Y. A., Hopmans, E. C., Meysman, F. J. R., Damsté, J. S. S., & Villanueva, L. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01661 · Cited by 937 · see citing works
Pii, Y., Mimmo, T., Tomasi, N., Terzano, R., Cesco, S., & Crecchio, C. (2015) · Biology and Fertility of Soils · doi:10.1007/s00374-015-0996-1 · Cited by 913 · see citing works
Bioremediation of soil contaminated with polynuclear aromatic hydrocarbons (PAHs): A review
Wilson, S. C., & Jones, K. C. (1993) · Environmental Pollution · doi:10.1016/0269-7491(93)90206-4 · Cited by 884 · see citing works
Studying plasmid horizontal transfer in situ: a critical review
Sørensen, S. J., Bailey, M., Hansen, L. H., Kroer, N., & Wuertz, S. (2005) · Nature Reviews Microbiology · doi:10.1038/nrmicro1232 · Cited by 726 · see citing works
Self-citationSoil enzymology: classical and molecular approaches
Nannipieri, P., Giagnoni, L., Renella, G., Puglisi, E., Ceccanti, B., Masciandaro, G., Fornasier, F., Moscatelli, M. C., & Marinari, S. (2012) · Biology and Fertility of Soils · doi:10.1007/s00374-012-0723-0 · Cited by 717 · see citing works
Self-citationGlobal biogeography of microbial nitrogen-cycling traits in soil
Albright, M., Martiny, A. C., & Martiny, J. B. H. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1601070113 · Cited by 572 · see citing works
Total bacterial diversity in soil and sediment communities—A review
Torsvik, V. L., Sørheim, R., & Goksøyr, J. (1996) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/bf01574690 · Cited by 513 · see citing works
The chemical and functional characterization of soil N and its biotic components
Nannipieri, P., & Paul, E. A. (2009) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2009.07.013 · Cited by 334 · see citing works
Self-citationStott, D. E., Andrews, S. S., Liebig, M. A., Wienhold, B. J., & Karlen, D. L. (2010) · Soil Science Society of America Journal · doi:10.2136/sssaj2009.0029 · Cited by 322 · see citing works
Microbiological methods for assessing soil quality
(2005) · CABI eBooks · doi:10.1079/9780851990989.0050 · Cited by 292 · see citing works
Luo, G., Ling, N., Nannipieri, P., Chen, H., Raza, W., Wang, M., Guo, S., & Shen, Q. (2017) · Biology and Fertility of Soils · doi:10.1007/s00374-017-1183-3 · Cited by 284 · see citing works
Self-citationBacterial ACC Deaminase and the Alleviation of Plant Stress
Glick, B. R. (2004) · Advances in applied microbiology · doi:10.1016/s0065-2164(04)56009-4 · Cited by 281 · see citing works
Wei, W., Isobe, K., Nishizawa, T., Zhu, L., Shiratori, Y., Ohte, N., Koba, K., Otsuka, S., & Senoo, K. (2015) · The ISME Journal · doi:10.1038/ismej.2015.9 · Cited by 275 · see citing works
Nitrogen turnover in soil and global change
Ollivier, J., Töwe, S., Bannert, A., et al. (2011) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2011.01165.x · Cited by 234 · see citing works
The ecology of transfer of mobile genetic elements
van Elsas, J. D., & Bailey, M. (2002) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2002.tb01008.x · Cited by 233 · see citing works
Bacterial conjugation between pseudomonads in the rhizosphere of wheat
van Elsas, J. D., Trevors, J. T., & Starodub, M. E. (1988) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1988.tb02676.x-i1 · Cited by 222 · see citing works
Lynch, J. M., Benedetti, A., Insam, H., Nuti, M., Smalla, K., Torsvik, V. L., & Nannipieri, P. (2004) · Biology and Fertility of Soils · doi:10.1007/s00374-004-0784-9 · Cited by 214 · see citing works
Self-citationPromoter clearance and escape in prokaryotes
Hsu, L. M. (2002) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/s0167-4781(02)00452-9 · Cited by 197 · see citing works
de Ridder-Duine, A. S., Kowalchuk, G. A., Gunnewiek, P. J. A. K., et al. (2004) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2004.08.005 · Cited by 191 · see citing works
Making big data smart—how to use metagenomics to understand soil quality
Vestergaard, G., Schulz, S., Schöler, A., & Schloter, M. (2017) · Biology and Fertility of Soils · doi:10.1007/s00374-017-1191-3 · Cited by 185 · see citing works
Self-citationBack to the Future of Soil Metagenomics
Nesme, J., Achouak, W., Agathos, S. N., et al. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00073 · Cited by 151 · see citing works
A review of molecular methods to study the microbiota of soil and the mycosphere
van Elsas, J. D., & Boersma, F. G. H. (2010) · European Journal of Soil Biology · doi:10.1016/j.ejsobi.2010.11.010 · Cited by 145 · see citing works
Nunes, I., Jacquiod, S., Brejnrod, A., Holm, P. E., Johansen, A., Brandt, K. K., Priemé, A., & Sørensen, S. J. (2016) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiw175 · Cited by 143 · see citing works
Self-citationLearning from agriculture: understanding low-dose antimicrobials as drivers of resistome expansion
You, Y., & Silbergeld, E. K. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00284 · Cited by 126 · see citing works
Lagos, L. M., Acuña, J. J., Maruyama, F., Ogram, A. V., Mora, M. D. L. L., & Jorquera, M. A. (2016) · Biology and Fertility of Soils · doi:10.1007/s00374-016-1137-1 · Cited by 122 · see citing works
Poulsen, P. H. B., Al‐Soud, W. A., Bergmark, L., Magid, J., Hansen, L. H., & Sørensen, S. J. (2012) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2011.12.023 · Cited by 119 · see citing works
Self-citationPlant Growth-Promoting Bacteria
van Elsas, J. D., Trevors, J. T., Jansson, J. K., et al. (2006) · CRC Press eBooks · doi:10.1201/9781420015201-27 · Cited by 108 · see citing works
Microbial remediation of aromatics-contaminated soil
Xu, Y., & Zhou, N. (2016) · Frontiers of Environmental Science & Engineering · doi:10.1007/s11783-017-0894-x · Cited by 89 · see citing works
Monitoring and evaluating soil quality.
Bloem, J., Schouten, A. J., Sørensen, S. J., Rutgers, M., van der Werf, A., & Breure, A. M. (2005) · CABI Publishing eBooks · doi:10.1079/9780851990989.0023 · Cited by 85 · see citing works
Self-citationRhizodeposition and Microbial Populations
Leij, F. A. A. M. D., Lynch, J. M., & Brimecombe, M. (2007) · Books in soils, plants, and the environment · doi:10.1201/9781420005585.ch3 · Cited by 85 · see citing works
Factors influencing variability of proteolytic genes and activities in arable soils
Fuka, M. M., Engel, M., Gattinger, A., et al. (2008) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2008.01.028 · Cited by 73 · see citing works
Microbe-mediated processes as indicators to establish the normal operating range of soil functioning
Silva, M. D. C. P. E., Semenov, A. V., Schmitt, H., van Elsas, J. D., & Salles, J. F. (2012) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2012.10.002 · Cited by 62 · see citing works
Uksa, M., Schloter, M., Endesfelder, D., et al. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.01269 · Cited by 61 · see citing works
Self-citationBaraniya, D., Puglisi, E., Ceccherini, M. T., et al. (2016) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2016.02.001 · Cited by 59 · see citing works
Shah, V., Zakrzewski, M., Wibberg, D., et al. (2013) · Microbial Ecology · doi:10.1007/s00248-013-0253-9 · Cited by 57 · see citing works
Bacterial conjugation between pseudomonads in the rhizosphere of wheat
VANELSAS, J., Trevors, J. T., & Starodub, M. E. (1988) · FEMS Microbiology Letters · doi:10.1016/0378-1097(88)90487-9 · Cited by 53 · see citing works
Self-citationCatechol and chlorocatechols in soil: Degradation and extractability
Cheng, H. H., Haider, K., & Harper, S. S. (1983) · Soil Biology and Biochemistry · doi:10.1016/0038-0717(83)90076-7 · Cited by 48 · see citing works
Plant-associated bacteria - lifestyle and molecular interactions
Sørensen, J., & Sessitsch, A. (2007) · Research at the University of Copenhagen (University of Copenhagen) · Cited by 48 · see citing works
The ecology of transfer of mobile genetic elements
VANELSAS, J., & Bailey, M. (2002) · FEMS Microbiology Ecology · doi:10.1016/s0168-6496(02)00373-2 · Cited by 43 · see citing works
Self-citationPathan, S. I., Ceccherini, M. T., Hansen, M. A., et al. (2015) · Biology and Fertility of Soils · doi:10.1007/s00374-015-1045-9 · Cited by 42 · see citing works
Haq, I. U., Graupner, K., Nazir, R., et al. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu126 · Cited by 33 · see citing works
Sukul, P., Schäkermann, S., Bandow, J. E., et al. (2017) · Microbiome · doi:10.1186/s40168-017-0247-9 · Cited by 27 · see citing works
Fuka, M. M., Engel, M., Haesler, F., et al. (2008) · Biology and Fertility of Soils · doi:10.1007/s00374-008-0319-x · Cited by 19 · see citing works
Quantitative assessment of soil functioning across a representative range of Dutch soils
Semenov, A. V., Silva, M. D. C. P. E., Salles, J. F., Schmitt, H., & van Elsas, J. D. (2014) · Ecological Indicators · doi:10.1016/j.ecolind.2013.11.009 · Cited by 19 · see citing works
Haq, I. U., Dini‐Andreote, F., & van Elsas, J. D. (2016) · Microbial Ecology · doi:10.1007/s00248-016-0885-7 · Cited by 18 · see citing works
Nannipieri, P., Pietramellara, G., & Renella, G. (2014) · Cited by 14 · see citing works
Self-citationErratum to: Diversity of Endosymbiotic Nostoc in Gunnera magellanica from Tierra del Fuego, Chile
Fernández-Martínez, M. Á., Rı́os, A. D. L., Sancho, L. G., et al. (2013) · Microbial Ecology · doi:10.1007/s00248-013-0244-x · Cited by 5 · see citing works
Flagged first, then by citations
Research works printed but not linked: 4
- Dini-Andreote F, Olff H, Van Elsas JD, Salles JF (2017) Metagenomics of microbiomes across a soil formation gradient. ISME J (in press)
- Emmerling C, Schloter M, Hartmann A, Kandeler E (2002) Functional diversity of soil organisms-a review of recent research activities in Germany. J Plant Nutr Soil Sci 165:408-420
- Prosser JI (2012) Nitrification. In: Huang PM, Li Y, Summer M (eds) Handbook of soil sciences. properties and processes, second Edition. Soil Biology and Biochemistry: soil biology in its second age Paul EA, Nannipieri P (Eds). CRC Press, Boca Raton, pp 27.19- 27.
- Van Elsas JD, Jansson JK, Trevors JT (2007) Modern Soil Microbiology II. CRC Press, Boca Raton
Cited by
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Soil quality – A critical review
Bünemann, E. K., Bongiorno, G., Bai, Z., Creamer, R. E., De Deyn, G., de Goede, R., Fleskens, L., Geissen, V., Kuyper, T. W., Mäder, P., et al. (2018) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2018.01.030 · Cited by 2,960 · see citing works
- Authors
- Schloter, M., Nannipieri, P., Sørensen, S. J., & van Elsas, J. D.
- Affiliations
- Helmholtz Munich (DE)
- University of Florence (IT)
- University of Copenhagen (DK)
- Venue
- Biology and Fertility of Soils
- Published
- 2017-10-16
- Volume
- 54
- Issue
- 1
- Pages
- 1-10
- ISSN
- 0178-2762 (ISSN-L)
- 1432-0789
- OpenAlex
- W2765364657
- Cited by
- 540
- References
- 61
- Citations by year
- 2026: 49 · 2025: 65 · 2024: 72 · 2023: 61 · 2022: 79 · 2021: 83 · 2020: 61 · 2019: 44 · 2018: 16 · 2015: 1 · 2014: 1 · 2013: 1 · 2012: 1
- FWCI
- 36.29
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Biology and Fertility of Soils (publishedVersion, cc-by)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by)
- mediaTUM – the media and publications repository of the Technical University Munich (Technical University Munich) (submittedVersion, other-oa)
- Site cant be reached (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
- PuSH - Publication Server of Helmholtz Zentrum München (submittedVersion)
- Funders
- University of Groningen
- 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 › Plant Science › Mycorrhizal Fungi and Plant Interactions
- Keywords
- soil quality, bioindicators, soil microbiome, keystone species, functional redundancy, molecular markers, soil functions, DNA-based methods, anthropogenic soil disturbance, climate change impacts on soil
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