Skip to main content
SpringerLink
Log in

Cattle impact on composition of archaeal, bacterial, and fungal communities by comparative fingerprinting of total and extracellular DNA

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

Abstract

The aim of the study was to evaluate the impact of cattle overwintering husbandry on composition of upland grassland soil archaeal, bacterial, and fungal communities by comparative fingerprinting (SSU rRNA denaturing gradient gel electrophoresis (DGGE)) of total (tDNA) and extracellular DNA (eDNA) extracted from three differently impacted soils (severely, moderately, and non-impacted soil) and cattle excrements. Cattle excrements carried a significant amount of viable microorganisms and eDNA, and as a result of its high external returns, the amounts of extractable eDNA in soil increased with cattle impact, being positively correlated with soil microbial biomass and activity. The soil eDNA fraction (2.8 to 5.7 μg g−1 dw) significantly contributed to the soil metagenome, representing 18–31 % of soil tDNA. The largest shift in soil community structure was observed for Archaea, followed by fungi and bacteria, indicating that soil bacteria possess the highest resilience to cattle-induced changes. Cattle excrements showed more diverse bacterial than archaeal and fungal communities. The specific DGGE bands of cattle excrements were also observed in community profiles of cattle-impacted soils, confirming the effect of cattle husbandry on composition of soil microbial communities, probably as a result of introduced rumen-borne microbes. Similar changes were also reflected in the eDNA-derived DGGE profiles, suggesting a higher contribution of bacteria to soil extracellular metagenome than Archaea and fungi. This study provided first evidences about the extracellular mobilome in cattle-impacted soils, carrying also genetic information of Archaea, and its susceptibility to impact by outdoor cattle husbandry.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Agnelli A, Ascher J, Corti G, Ceccherini MT, Nannipieri P, Pietramellara G (2004) Distribution of microbial communities in a forest soil profile investigated by microbial biomass, soil respiration and DGGE of total and extracellular DNA. Soil Biol Biochem 36:859–868

    Article  CAS  Google Scholar 

  • Agnelli A, Ascher J, Corti G, Ceccherini MT, Pietramellara G, Nannipieri P (2007) Purification and isotopic signatures (δ13C, δ15N, Δ14C) of soil extracellular DNA. Biol Fertil Soils 44:353–361

    Article  CAS  Google Scholar 

  • Ascher J, Ceccherini MT, Pantani OL, Agnelli A, Borgogni F, Guerri G, Nannipieri P, Pietramellara G (2009a) Sequential extraction and genetic fingerprinting of a forest soil metagenome. Appl Soil Ecol 42:176–181

    Article  Google Scholar 

  • Ascher J, Ceccherini MT, Landi L, Mench M, Pietramellara G, Nannipieri P, Renella G (2009b) Composition, biomass and activity of micro-flora, and leaf yields and foliar elemental concentrations of lettuce, after in situ stabilization of an arsenic-contaminated soil. Appl Soil Ecol 41:351–359

    Article  Google Scholar 

  • Auguet JC, Barberan A, Casamayor EO (2010) Global ecological patterns in uncultured Archaea. ISME J 4:182–190

    Article  PubMed  Google Scholar 

  • Bihn CTT, Heuer H, Kaupenjohann M, Smalla K (2008) Piggery manure used for soil fertilization is a reservoir for transferable antibiotic resistance plasmids. FEMS Microbiol Ecol 66:25–37

    Article  Google Scholar 

  • Bolton DJ, Monaghan A, Byrne B, Fanning S, Sweeney T, McDowell DA (2011) Incidence and survival of non-O157 verocytotoxigenic Escherichia coli in soil. J Appl Microbiol 111:484–490

    Article  PubMed  CAS  Google Scholar 

  • Ceccherini MT, Ascher J, Pietramellara G, Nannipieri P (2007) Vertical advection of extracellular DNA by water capillarity in soil columns. Soil Biol Biochem 39:158–163

    Article  CAS  Google Scholar 

  • Ceccherini MT, Ascher J, Agnelli A, Borgogni F, Pantani OL, Pietramellara G (2009a) Experimental discrimination and molecular characterization of the extracellular soil DNA fraction. Anton Leeuw Int J G 96:653–657

    Article  CAS  Google Scholar 

  • Ceccherini MT, Ascher J, Guerri G, Pietramellara G (2009b) In-field detection and quantification of extracellular DNA. J Plant Nutr Soil Sci 172:626–629

    Article  CAS  Google Scholar 

  • Chemidlin Prèvost-Bourè N, Christen R, Dequiedt S, Mougel C, Lelièvre M, Jolivet C, Shahbazkia HR, Guillou L, Arrouays D, Ranjard L (2011) Validation and application of a PCR primer set to quantify fungal communities in the soil environment by real-time quantitative PCR. PLoS One 6:e24166

    Article  PubMed  Google Scholar 

  • Chroňáková A, Radl V, Čuhel J, Šimek M, Elhottová D, Engel M, Schloter M (2009) Overwintering management on upland pasture causes shift in the abundance of denitrifying microbial communities, the activity and N2O producing ability. Soil Biol Biochem 41:1132–1138

    Article  Google Scholar 

  • Coolen MJL, Hopmans EC, Rijpstra WIC, Muyzer G, Schoulen S, Volkman JK, Damsté JSS (2004) Evolution of the methane cycle in Ace Lake (Antarctica) during the Holocene: response of methanogens and methanotrophs to environmental change. Org Geochem 35:1151–1167

    Article  CAS  Google Scholar 

  • Corinaldesi C, Beolchini F, Dell’Anno A (2008) Damage and degradation rates of extracellular DNA in marine sediemnts: implications for the preservation of gene sequeces. Mol Ecol 17:3939–3951

    Article  PubMed  CAS  Google Scholar 

  • de Vries J, Wackernagel W (2004) Microbial horizontal gene transfer and the DNA release from transgenic crop plants. Plant Soil 266:91–104

    Article  Google Scholar 

  • Elhottová D, Koubová A, Šimek M, Cajthaml T, Jirout J, Esperschütz J, Schloter M, Gattinger A (2012) Changes in soil microbial communities as affected by intensive cattle husbandry. Appl Soil Ecol 58:56–65

    Article  Google Scholar 

  • Ettema TJG, Andersson SGE (2009) The α-Proteobacteria: the Darwin finches of the bacterial world. Biol Lett 5:429–432

    Article  PubMed  Google Scholar 

  • Friedlander AM (1975) DNA release as a direct measure of microbial killing I. Serum bactericidal activity. J Immunol 115:1404–1408

    PubMed  CAS  Google Scholar 

  • Girvan MS, Bullimore J, Pretty JN, Osborn AM, Ball AS (2003) Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Appl Environ Microbiol 69:1800–1809

    Article  PubMed  CAS  Google Scholar 

  • Green SJ, Leigh MB, Neufeld JD (2009) Denaturing gradient gel electrophoresis (DGGE) for microbial community analysis. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Heidelberg, pp 4137–4158

    Google Scholar 

  • Herdina NS, Jabaji-Hare S, Ophel-Keller K (2004) Persistence of DNA of Gaeumannomyces graminis var. tritici in soil as measured by a DNA-based assay. FEMS Microbiol Ecol 47:143–152

    Article  PubMed  CAS  Google Scholar 

  • Hynšt J, Šimek M, Brůček P, Petersen SO (2007) High fluxes but different patterns of nitrous oxide and carbon dioxide emissions from soil in a cattle overwintering area. Agr Ecosys Environ 120:269–279

    Article  Google Scholar 

  • Janssen HP, Kirs M (2008) Structure of archaeal community of the rumen. Appl Environ Microbiol 74:3619–3625

    Article  PubMed  CAS  Google Scholar 

  • Jirout J, Šimek M, Elhottová D (2011) Inputs of nitrogen and organic matter govern the composition of fungal communities in soil disturbed by overwintering cattle. Soil Biol Biochem 43:647–656

    Article  CAS  Google Scholar 

  • Johnsborg O, Eldholm V, Håvarstein S (2007) Natural genetic transformation: prevalence, mechanisms and function. Res Microbiol 158:767–778

    Article  PubMed  CAS  Google Scholar 

  • Kim M, Morrison M, Yu Z (2011) Status of the phylogenetic diversity census of ruminal microbiomes. FEMS Microbiol Ecol 76:49–63

    Article  PubMed  CAS  Google Scholar 

  • Koonin EV, Wolf YI (2008) Genomics of bacteria and Archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res 36:6688–6719

    Article  PubMed  CAS  Google Scholar 

  • Koubová A, Goberna M, Šimek M, Chroňáková A, Pižl V, Insam H, Elhottová D (2012) Effects of the earthworm Eisenia andrei on methanogens in a cattle-impacted soil: a microcosm study. Eur J Soil Biol 48:32–40

    Article  Google Scholar 

  • Kozdrój J, Van Elsas DJ (2000) Application of polymerase chain reaction denaturing gradient gel electrophoresis for comparison of direct and indirect extraction methods of soil DNA used for microbial community fingerprinting. Biol Fert Soil 31:372–378

    Article  Google Scholar 

  • Lehtovirta LE, Prosser JI, Nicol GW (2009) Soil pH regulates the abundance and diversity of group 1.1c Crenarchaeota. FEMS Microb Ecol 70:367–376

    Article  CAS  Google Scholar 

  • Levy SB (2002) The antibiotic paradox: how the misuse of antibiotics destroys their curative powers. Da Copo Press, Perseus Publishing, USA, p 312

    Google Scholar 

  • Levy-Both D, Campbell RG, Gulden RH, Hart MM, Powell R, Klironomos JN, Pauls KP, Swanton CJ, Trevors JT, Dunfield KE (2007) Cycling of extracellular DNA in the soil environment. Soil Biol Biochem 39:2977–2991

    Article  Google Scholar 

  • Marstorp H, Witter E (1999) Extractable dsDNA and product formation as measures of microbial growth in soil upon substrate addition. Soil Biol Biochem 31:1443–1453

    Article  CAS  Google Scholar 

  • Muella A, Arana I, Justo JI, Seco C, Barcina I (1999) Changes in DNA content and cellular death during a starvation-survival process of Escherichia coli in river water. Microb Ecol 37:62–69

    Article  Google Scholar 

  • Nacke H, Thürmer A, Wollherr A, Will C, Hodac L, Herold N, Schöning I, Schrupf M, Daniel R (2011) Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS One 6:e17000

    Article  PubMed  CAS  Google Scholar 

  • Naya H, Romero H, Zavala A, Alvarez B, Musto H (2002) Aerobiosis increases the genomic guanine plus cytosine content (GC%) in prokaryotes. J Mol Evol 55:260–264

    Article  PubMed  CAS  Google Scholar 

  • Nicol GW, Glover LA, Prosser JI (2003) The impact of grassland management on archaeal community structure in upland pasture rhizosphere soil. Environ Microbiol 5:152–162

    Article  PubMed  CAS  Google Scholar 

  • Nielsen KM, Johnsen PJ, Bensasson D, Daffonchio D (2007) Release and persistence of extracellular DNA in the environment. Environ Biosafety Res 6:37–53

    Article  PubMed  CAS  Google Scholar 

  • Nübel U, Engelen B, Felske A, Snaidr J, Wieshuber A, Amann RI, Ludwig W, Backhaus H (1996) Sequence heterogeneities of genes encoding 16 S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol 178:5636–5643

    PubMed  Google Scholar 

  • Orpin CG, Joblin KN (1997) The rumen anaerobic fungi. In: Hobson PN, Steward CS (eds) The rumen microbial ecosystem. Chapman & Hall, London, pp 140–195

    Chapter  Google Scholar 

  • Paget E, Simonet P (1994) On the track of natural transformation in soil. FEMS Microbiol Ecol 15:109–118

    Article  CAS  Google Scholar 

  • Pester M, Schleper C, Wagner M (2011) The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr Opin Microbiol 14:300–306

    Article  PubMed  CAS  Google Scholar 

  • Philippot L, Bru D, Saby NPA, Čuhel J, Arrouyas D, Šimek M, Hallin S (2009) Spatial patterns of bacterial taxa in nature reflect ecological traits of deep branches of the 16 S rRNA bacterial tree. Environ Microbiol 11:3096–3104

    Article  PubMed  CAS  Google Scholar 

  • Pietramellara G, Ceccherini MT, Ascher J, Nannipieri P (2006) Persistence of transgenic and not transgenic extracellular DNA in soil and bacterial transformation. Riv Biol 99:37–68

    PubMed  Google Scholar 

  • Pietramellara G, Ascher J, Borgogni F, Ceccherini MT, Guerri G, Nannipieri P (2009) Extracellular DNA in soil and sediment: fate and ecological relevance. Biol Fertil Soils 45:219–235

    Article  CAS  Google Scholar 

  • Radl V, Gattinger A, Chroňáková A, Němcová A, Čuhel J, Šimek M, Munch JC, Schloter M, Elhottová D (2007) Effects of cattle husbandry on abundance and activity of methanogenic Archaea in upland soils. ISME J 1:443–452

    Article  PubMed  CAS  Google Scholar 

  • Rajendhran J, Gunasekaran P (2008) Strategies for accessing soil metagenome for desired applications. Biotechnol Adv 26:576–590

    Article  PubMed  CAS  Google Scholar 

  • Recorbet G, Picard C, Normand P, Simonet P (1993) Kinetics of persistence of chromosomal DNA from genetically engineered Escherichia coli introduced into soil. Appl Environ Microbiol 59:4289–4294

    PubMed  CAS  Google Scholar 

  • Vainio EJ, Hantula J (2000) Direct analysis of wood-inhabiting fungi using denaturing gradient gel electrophoresis of amplified ribosomal DNA. Mycol Res 104:927–936

    Article  CAS  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Wackernagel W (2006) The various sources and the fate of nucleic acids in soil. In: Nannipieri P, Smalla K (eds) Nucleic acids and proteins in soil. Springer, Berlin, pp 117–139

    Chapter  Google Scholar 

  • Wardle DA, Ghani A (1995) A critique of the microbial metabolic quotient (qCO2) as a bioindicator of disturbance and ecosystem development. Soil Biol Biochem 27:1601–1610

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The research was supported by the Czech Science Foundation (No 526/09/1570 and P504/10/2077), the Ministry of Education, Youth and Sports of the Czech Republic (LC06066), and the Ente Cassa di Risparmio di Firenze. L. Jíšová is greatly acknowledged for field work and laboratory analyses. Mr. and Mrs. Kamír are thanked for allowing access to the experimental plot and their significant support of the field work.

Author information

Authors and Affiliations

  1. Institute of Soil Biology, Biology Centre AS CR, v. v. i., Na Sádkách 7, 370 05, České Budějovice, Czech Republic

    A. Chroňáková, J. Jirout, D. Elhottová & M. Šimek

  2. Department of Plant, Soil and Environmental Sciences, University of Firenze, Piazzale delle Cascine 18, 50144, Florence, Italy

    J. Ascher, M. T. Ceccherini & G. Pietramellara

  3. Faculty of Science, University of South Bohemia, Branišovská 31, 370 05, České Budějovice, Czech Republic

    M. Šimek

Authors
  1. A. Chroňáková
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Ascher
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Jirout
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. T. Ceccherini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. D. Elhottová
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. G. Pietramellara
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Šimek
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Chroňáková.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

(JPEG 138 kb)

High resolution image file (TIFF 1.40 MB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chroňáková, A., Ascher, J., Jirout, J. et al. Cattle impact on composition of archaeal, bacterial, and fungal communities by comparative fingerprinting of total and extracellular DNA. Biol Fertil Soils 49, 351–361 (2013). https://doi.org/10.1007/s00374-012-0726-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-012-0726-x

Keywords

Search

Navigation