Skip to main content
SpringerLink
Log in

Endospores, prokaryotes, and microbial indicators in arable soils from three long-term experiments

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

Management impacts on microbial communities in arable soil may influence soil quality and fertility. We examined the composition of the prokaryotic community in soils maintained under specific treatments for 24–118 years at Askov Experimental Station, Denmark. The experiments involved nutrient addition (unfertilized, mineral fertilizer, cattle manure), straw disposal (no straw, 8 t straw ha−1 year−1), and soil texture (5–18 % clay). Domain- and phylum-assigned cells were quantified by 16S ribosomal RNA (rRNA) gene analysis and endospores by analysis of dipicolinic acid (DPA). Amino sugars (glucosamine, galactosamine, and muramic acid) were assayed as microbial source indicators. Severe nutrient depletion reduced cell numbers and increased endospore abundance; straw disposal slightly increased both prokaryote and endospore numbers. Nutrient source (animal manure or mineral fertilizer) and soil texture had a little effect on cell and endospore numbers. With the notable exception of unfertilized soil, the ratio of endospores to total cells was similar across all treatments. The 16S rRNA gene analysis showed dominance of Bacteria over Archaea, the latter accounting for 0.2–8.4 % of total genes. Archaeal abundance differed a little among treatments. Firmicutes made up 0.2–1.2 % of the bacterial 16S rRNA genes. The numbers of Firmicutes were lower in unfertilized than in fertilized soil and decreased with decreasing soil clay content; straw treatment and nutrient source had a little effect. Amino sugar ratios suggested a dominance of fungi over bacteria, but the concentrations of microbial indicators and soil organic C were closely correlated, indicating that the amino sugar ratios represented a historical fingerprint (legacy effect) of the impact of management on the microbial community. Our results show that it takes extreme management to distort the general structure of prokaryotic communities in temperate arable soils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Acosta-Martínez V, Dowd S, Sun Y, Allen V (2008) Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biol Biochem 40:2762–2770

    Article  CAS  Google Scholar 

  • Amelung W, Brodowski S, Sandhage-Hofmann A, Bol R (2008) Combining biomarker with stable isotope analyses for assessing the transformation and turnover of soil organic matter. Adv Agron 100:155–250

    Article  CAS  Google Scholar 

  • Ammann AB, Kölle L, Brandl H (2011) Detection of bacterial endospores in soil by terbium fluorescence. Int J Microbiol 2011: Article ID 435281, 5 pp

  • Bacchetti De Gregoris T, Aldred N, Clare AS, Burgess JG (2011) Improvement of phylum- and class-specific primers for real-time PCR quantification of bacterial taxa. J Microbiol Methods 8:351–356

    Article  CAS  Google Scholar 

  • Bakken LR, Frostegard A (2006) Nucleic acid extraction from soil. In: Nannipieri P, Smalla K (Eds) Nucleic acids and proteins in soil. Soil biology, 8th edn. Springer, Berlin, pp 49–73

  • Bengtson P, Sterngren AE, Rousk J (2012) Archaeal abundance across a pH gradient in an arable soil and its relationship to bacterial and fungal growth rates. Appl Environ Microbiol 78:5906–5911

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bissett A, Richardson AE, Baker G, Thrall PH (2011) Long-term land use effects on soil microbial community structure and function. Appl Soil Ecol 51:66–78

    Article  Google Scholar 

  • Börjesson G, Menichetti L, Kirchmann H, Kätterer T (2012) Soil microbial community structure affected by 53 years of nitrogen fertilisation and different organic amendments. Biol Fertil Soils 48:245–257

    Article  CAS  Google Scholar 

  • Cadillo-Quiroz H, Bräuer S, Yashiro E, Sun C, Yavitt J, Zinder S (2006) Vertical profiles of methanogenesis and methanogens in two contrasting acidic peatlands in central New York State, USA. Environ Microbiol 8:1428–1440

    Article  PubMed  CAS  Google Scholar 

  • Christensen BT, Bech-Andersen S (1989) Influence of straw disposal on distribution of amino acids in soil particle size fractions. Soil Biol Biochem 21:35–40

    Article  CAS  Google Scholar 

  • Christensen BT, Petersen J, Trentemøller U (2006) The Askov long-term experiments on animal manure and mineral fertilizers: the Lermarken site 1894–2004. DIAS Report Plant Production no. 121, April 2006, Danish Institute of Agricultural Sciences, Tjele, Denmark, pp. 104

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

  • Daims H, Bruhl A, Amann R, Schleifer KH, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434–444

    Article  PubMed  CAS  Google Scholar 

  • Enwall K, Nyberg K, Bertilsson S, Cederlund H, Stenström J, Hallin S (2007) Long-term impact of fertilization on activity and composition of bacterial communities and metabolic guilds in agricultural soil. Soil Biol Biochem 39:106–115

    Article  CAS  Google Scholar 

  • Fetzner S (1998) Bacterial degradation of pyridine, indole, quinolone, and their derivatives under different redox conditions. Appl Microbiol Biotechnol 49:237–350

    Article  CAS  Google Scholar 

  • Fichtel J, Köster J, Rullkötter J, Sass H (2007) Spore dipicolinic acid contents used for estimating the number of endospores in sediments. FEMS Microbiol Ecol 61:522–532

    Article  PubMed  CAS  Google Scholar 

  • Fichtel J, Köster J, Rullkötter J, Sass H (2008) High variations in endospore numbers within tidal flat sediments revealed by quantification of dipicolinic acid. Geomicrobiol J 25:371–380

    Article  CAS  Google Scholar 

  • Filippidou S, Junier T, Wunderlin T, Lo C-C, Li P-E, Chain PS, Junier P (2015) Under-detection of endospore-forming Firmicutes in metagenomics data. Comp Struc Biotech J 13:299–306

    Article  Google Scholar 

  • Girvan MS, Bullimore J, Ball AS, Pretty JN, Osborn AM (2004) Responses of active bacterial and fungal communities in soils under winter wheat to different fertilizer and pesticide regimens. Appl Environ Microbiol 70:2692–2701

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hartmann M, Fliessbach A, Oberholzer H-R, Widmer F (2006) Ranking the magnitude of crop and farming system effects on soil microbial biomass and genetic structure of bacterial communities. FEMS Microbiol Ecol 57:378–388

    Article  PubMed  CAS  Google Scholar 

  • Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Joergensen RG, Wichern F (2008) Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biol Biochem 40:2977–2991

    Article  CAS  Google Scholar 

  • Johnson MJ, Lee KY, Scow KM (2003) DNA fingerprinting reveals links among agricultural crops, soil properties, and the composition of soil microbial communities. Geoderma 114:279–303

    Article  Google Scholar 

  • Kallmeyer J, Smith DC, Spivack AJ, D’Hondt S (2008) New cell extraction procedure applied to deep subsurface sediments. Limnol Oceanogr Meth 6:236–245

    Article  Google Scholar 

  • Karlsson AE, Johansson T, Bengtson P (2012) Archaeal abundance in relation to root and fungal exudation rates. FEMS Microbiol Ecol 80:305–311

    Article  PubMed  CAS  Google Scholar 

  • Kristiansen SM, Hansen EM, Jensen LS, Christensen BT (2005) Natural 13C abundance and carbon storage in Danish soils under continuous silage maize. Eur J Agron 22:107–117

    Article  CAS  Google Scholar 

  • Langerhuus AT, Røy H, Lever MA, Morono Y, Inagaki F, Jørgensen BB, Lomstein BA (2012) Endospore abundance and D:L-amino acid modeling of bacterial turnover in Holocene marine sediment (Aarhus Bay). Geochim Cosmochim Acta 99:87–99

    Article  CAS  Google Scholar 

  • Lindroth P, Mopper K (1979) High performance liquid chromatographic determination of subpicomole amounts of amino-acids by precolumn fluorescence derivatization with o-phthaldialdehyde. Anal Chem 51:1667–1674

    Article  CAS  Google Scholar 

  • Lomstein BA, Jørgensen BB (2012) Pre-column liquid chromatographic determination of dipicolinic acid from bacterial endospores. Limnol Oceanogr Meth 10:227–233

    Article  CAS  Google Scholar 

  • Lomstein BA, Langerhuus AT, D’Hondt S, Jørgensen BB, Spivack AJ (2012) Endospore abundance, microbial growth and necromass turnover in deep sub-seafloor sediment. Nature 484:101–104

    Article  PubMed  CAS  Google Scholar 

  • Loy A, Lehner A, Lee N, Adamczyk J, Meier H, Ernst J, Schleifer KH, Wagner M (2002) Oligonucleotide microarray for 16S rRNA gene-based detection of all recognized lineages of sulfate-reducing prokaryotes in the environment. Appl Environ Microbiol 68:5064–5081

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lunau M, Lemke A, Walther K, Martens-Habbena W, Simon M (2005) An improved method for counting bacteria from sediments and turbid environments by epifluorescence microscopy. Environ Microbiol 7:961–968

    Article  PubMed  Google Scholar 

  • Murugan R, Kumar S (2013) Influence of long-term fertilisation and crop rotation on changes in fungal and bacterial residues in a tropical rice-field soil. Biol Fertil Soils 49:847–856

    Article  Google Scholar 

  • Myrold DD, Nannipieri P (2014) Classical techniques versus omics approaches. In: Nannipieri P, Pietramellara G, Renella G (Eds) Omics in soil science. Caster Academy Press, Norfolk, pp 179–187

  • Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670

    Article  Google Scholar 

  • Neumann D, Heuer A, Hemkemeyer M, Martens R, Tebbe CC (2013) Response of microbial communities to long-term fertilization depends on their microhabitat. FEMS Micobiol Ecol 86:71–84

    Article  CAS  Google Scholar 

  • Ogilvie LA, Hirsch PR, Johnston AWB (2008) Bacterial diversity of the Broadbalk Classical Winter Wheat Experiment in relation to long-term fertilizer inputs. Microb Ecol 56:525–537

    Article  PubMed  Google Scholar 

  • Ollivier J, Töwe S, Bannert A, Hai B, Kastl E-M, Meyer A, Su MX, Kleineidam K, Schloter M (2011) Nitrogen turnover in soil and global change. FEMS Microbiol Ecol 78:3–16

    Article  PubMed  CAS  Google Scholar 

  • Paterson E, Sim A, Osborne SM, Murray PJ (2011) Long-term exclusion of plant-inputs to soil reduces the functional capacity of microbial communities to mineralise root-derived carbon sources. Soil Biol Biochem 43:1873–1880

    Article  CAS  Google Scholar 

  • Paul EA (ed) (2015) Soil microbiology, ecology and biochemistry, 4th edn. Academic, London

    Google Scholar 

  • Pereira-e-Silva MC, Dias ACF, van Elsas JD, Salles JF (2012) Spatial and temporal variation of archaeal, bacterial and fungal communities in agricultural soils. PLoS One 7, e51554. doi:10.1371/journal.pone.0051554

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Portillo MC, Leff JW, Lauber CL, Fierer N (2013) Cell size distribution of soil bacteria and archaeal taxa. Appl Environ Microbiol 79:7610–7617

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Poulsen PHB, Al-Soud WA, Bergmark L, Magid J, Hansen LH, Sørensen SJ (2013) Effects of fertilization with urban and agricultural organic wastes in a field trial—prokaryotic diversity investigated by pyrosequencing. Soil Biol Biochem 57:784–793

    Article  CAS  Google Scholar 

  • Rodríguez-Blanco A, Sicardi M, Frioni L (2015) Plant genotype and nitrogen fertilization effects on abundance and diversity of diazotrophic bacteria associated with maize (Zea mays L.). Biol Fertil Soils 51:391–402

    Article  CAS  Google Scholar 

  • Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351

    Article  PubMed  Google Scholar 

  • Schjønning P, Elmholt S, Christensen BT (eds) (2004) Managing soil quality—challenges in modern agriculture. CAB International, Wallingford

    Google Scholar 

  • Shen Z, Ruan Y, Chao X, Zhang J, Li R, Shen Q (2015) Rhizosphere microbial community manipulated by 2 years of consecutive biofertilizer application associated with banana Fusarium wilt disease suppression. Biol Fertil Soils 51:553–562

    Article  CAS  Google Scholar 

  • Stoddard SF, Smith BJ, Hein R, Roller BRK, Schmidt TM (2014) rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nuc Acid Res 43:D593–D598. doi:10.1093/nar/gku1201

    Article  Google Scholar 

  • Thomsen IK, Christensen BT (2004) Yields of wheat and soil carbon and nitrogen contents following long-term incorporation of barley straw and ryegrass catch crops. Soil Use Manag 20:432–438

    Article  Google Scholar 

  • Ulrich A, Becker R (2006) Soil parent material is a key determinant of the bacterial community structure in arable soils. FEMS Microbiol Ecol 56:430–443

    Article  PubMed  CAS  Google Scholar 

  • Yin C, Jones KL, Peterson DE, Garrett KA, Hulbert SH, Paulitz TC (2010) Members of soil bacterial communities sensitive to tillage and crop rotation. Soil Biol Biochem 42:2111–2118

    Article  CAS  Google Scholar 

  • Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89:670–679

    Article  PubMed  CAS  Google Scholar 

  • Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84:2042–2050

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the Mexican Research Council (CONACyT), PhD grant number 213154. The contribution of B.T.C. and L.E. and field experiments at Askov Experimental Station were financially supported by the EU-FP7 project SmartSOIL (Grant No. 289694). The research underlying this article has been cofunded by the Danish National Research Foundation and the European Research Council under the EU-FP7 (ERC Grant No. 294200). We acknowledge Lykke Poulsen, Susanne Nielsen, Jeanette Pedersen, Karina B. Henriksen, Trine B. Søgaard, and the staff at Askov Experimental Station for their excellent technical support.

Author information

Author notes

  1. Paulina Tamez-Hidalgo

    Present address: Department for Animal Health and Nutrition, Novozymes A/S, Krogshøjvej 36, DK-2880, Bagsvaerd, Denmark

Authors and Affiliations

  1. Department of Bioscience, Section for Microbiology, Aarhus University, Ny Munkegade 114, DK-8000, Aarhus C, Denmark

    Paulina Tamez-Hidalgo & Bente Aa. Lomstein

  2. Department of Agroecology, Aarhus University, AU-Foulum, DK-8830, Tjele, Denmark

    Bent T. Christensen & Lars Elsgaard

  3. Department of Bioscience, Center for Geomicrobiology, Aarhus University, DK-8000, Aarhus C, Denmark

    Mark A. Lever & Bente Aa. Lomstein

  4. Department of Environmental Systems Sciences, Institute for Biogeochemistry and Pollutant Dynamics, ETH Zurich, CH-8092, Zurich, Switzerland

    Mark A. Lever

Authors
  1. Paulina Tamez-Hidalgo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bent T. Christensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mark A. Lever
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lars Elsgaard
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bente Aa. Lomstein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bente Aa. Lomstein.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tamez-Hidalgo, P., Christensen, B.T., Lever, M.A. et al. Endospores, prokaryotes, and microbial indicators in arable soils from three long-term experiments. Biol Fertil Soils 52, 101–112 (2016). https://doi.org/10.1007/s00374-015-1057-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-015-1057-5

Keywords

Search

Navigation