Skip to main content
Log in

In Situ Dynamics of Microbial Communities during Decomposition of Wheat, Rape, and Alfalfa Residues

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Microbial communities are of major importance in the decomposition of soil organic matter. However, the identities and dynamics of the populations involved are still poorly documented. We investigated, in an 11-month field experiment, how the initial biochemical quality of crop residues could lead to specific decomposition patterns, linking biochemical changes undergone by the crop residues to the respiration, biomass, and genetic structure of the soil microbial communities. Wheat, alfalfa, and rape residues were incorporated into the 0–15 cm layer of the soil of field plots by tilling. Biochemical changes in the residues occurring during degradation were assessed by near-infrared spectroscopy. Qualitative modifications in the genetic structure of the bacterial communities were determined by bacterial-automated ribosomal intergenic spacer analysis. Bacterial diversity in the three crop residues at early and late stages of decomposition process was further analyzed from a molecular inventory of the 16S rDNA. The decomposition of plant residues in croplands was shown to involve specific biochemical characteristics and microbial community dynamics which were clearly related to the quality of the organic inputs. Decay stage and seasonal shifts occurred by replacement of copiotrophic bacterial groups such as proteobacteria successful on younger residues with those successful on more extensively decayed material such as Actinobacteria. However, relative abundance of proteobacteria depended greatly on the composition of the residues, with a gradient observed from alfalfa to wheat, suggesting that this bacterial group may represent a good indicator of crop residues degradability and modifications during the decomposition process.

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

Access this article

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

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. Albrecht R, Joffre R, Gros R, Le Petit J, Terrom G, Périssol C (2008) Efficiency of near-infrared reflectance spectroscopy to assess and predict the stage of transformation of organic matter in the composting process. Bioresour Technol 99:448–455

    Article  CAS  PubMed  Google Scholar 

  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  3. Amann RI, Ludwig W, Schleifer K-H (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169

    CAS  PubMed  Google Scholar 

  4. Aneja MK, Sharma S, Fleischmann F, Stich S, Heller W, Bahnweg G, Munch JC, Schloter M (2006) Microbial colonization of beech and spruce litter—influence of decomposition site and plant litter species on the diversity of microbial community. Microb Ecol 52:127–135

    Article  PubMed  Google Scholar 

  5. Bastian F, Bouziri L, Nicolardot B, Ranjard L (2009) Impact of wheat straw decomposition on successional patterns of soil microbial community structure. Soil Biol Biochem 41:262–275

    Article  CAS  Google Scholar 

  6. Baumann K, Marschner P, Smernik RJ, Baldock JA (2009) Residue chemistry and microbial community structure during decomposition of eucalypt, wheat and vetch residues. Soil Biol Biochem 41:1966–1975

    Article  CAS  Google Scholar 

  7. Bernard L, Mougel C, Maron PA, Nowak V, Henault C, Lévêque J, Haichar F, Berge O, Marol C, Balesdent J, Gibiat F, Lemanceau P, Ranjard L (2007) Dynamics and identification of microbial populations involved in the decomposition of 13C labelled wheat residue as estimated by DNA- and RNA-SIP techniques. Environ Microbiol 9:752–764

    Article  CAS  PubMed  Google Scholar 

  8. Buchan A, Newell SY, Butler M, Biers EJ, Hollibaugh JT, Moran MA (2003) Dynamics of bacterial and fungal communities on decaying salt marsh grass. Appl Environ Microbiol 69:6676–6687

    Article  CAS  PubMed  Google Scholar 

  9. Campbell CA, Zentner RP, Selles F, Biederbeck VO (2000) Quantifying short-term effects of crop rotations on soil organic carbon in Southwestern Saskatchewan. Can J Soil Sci 80:193–202

    Google Scholar 

  10. Cayuela ML, Sinicco T, Mondini C (2009) Mineralization dynamics and biochemical properties during initial decomposition of plant and animal residues in soil. Appl Soil Ecol 41:118–127

    Article  Google Scholar 

  11. Cécillon L, Cassagne N, Czarnes S, Gros R, Vennetier M, Brun JJ (2009) Predicting soil quality indices with near infrared analysis in a wildfire chronosequence. Sci Total Environ 407:1200–1205

    Article  PubMed  Google Scholar 

  12. Cécillon L, de Mello NA, De Danieli S, Brun JJ (2010) Soil macroaggregate dynamics in a mountain spatial climate gradient. Biogeochemistry 97:31–43

    Article  Google Scholar 

  13. Charron CS, Sams CE (1999) Inhibition of Pythium ultimum and Rhizoctonia solani by shredded leaves of Brassica species. J Am Soc Hortic Sci 124:462–467

    CAS  Google Scholar 

  14. Chessel D, Dufour AB, Thioulouse J (2004) The ade4 package—I: one-table methods. R News 4:5–10

    Google Scholar 

  15. Chodak M (2008) Application of near infrared spectrometry for analysis of soils, litter and plant materials. Pol J Environ Stud 17:631–642

    CAS  Google Scholar 

  16. Coppens F, Garnier P, De Gryze S, Merckx R, Recous S (2006) Soil moisture, carbon and nitrogen dynamics following incorporation and surface application of labelled crop residues in soil columns. Eur J Soil Sci 57:894–905

    Article  CAS  Google Scholar 

  17. De Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811

    Article  PubMed  Google Scholar 

  18. Demetz M, Insam H (1999) Phosphorus availability in a forest soil determined with a respiratory assay compared to chemical methods. Geoderma 89:259–271

    Article  CAS  Google Scholar 

  19. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364

    Article  PubMed  Google Scholar 

  20. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  21. Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial question? Soil Biol Biochem 35:837–843

    Article  CAS  Google Scholar 

  22. Fourty T, Baret F, Jacquemoud S, Schmuck G, Verdebout J (1996) Leaf optical properties with explicit description of its biochemical composition: direct and inverse problems. Remote Sens Environ 56:104–117

    Article  Google Scholar 

  23. Fredrickson JK, Balkwill DL, Drake GR, Romine MF, Ringelberg DB, White DC (1995) Aromatic-degrading Sphingomonas isolate from deep subsurface. Appl Environ Microbiol 61:1917–1922

    CAS  PubMed  Google Scholar 

  24. Giller KE, Witter E, McGrath SE (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414

    Article  CAS  Google Scholar 

  25. Gleixner G, Czimczik CJ, Kramer C, Lühker B, Schmidt MWI (2001) Plant compounds and their turnover and stability as soil organic matter. In: Schulze ED, Heimann M, Harrison S, Holland E, Lloyd JL, Prentice C, Schimel D (eds) Global biogeochemical cycles in the climate system. Academic Press, San Diego, pp 201–215

    Chapter  Google Scholar 

  26. Holland EA, Coleman DC (1987) Litter placement effects on microbial and organic-matter dynamics in an agrosystem. Ecology 68:425–433

    Article  Google Scholar 

  27. Jensen LS, Salo T, Palmason F, Breland TA, Henriksen TM, Stenberg B, Pedersen A, Lundström C, Esala M (2005) Influence of biochemical quality on C and N mineralisation from a broad variety of plant materials in soil. Plant Soil 273:307–326

    Article  CAS  Google Scholar 

  28. Joffre R, Gillon D, Dardenne P, Agneessens R, Biston R (1992) The use of near-infrared reflectance spectroscopy in litter decomposition studies. Ann Sci For 49:481–488

    Article  Google Scholar 

  29. Kimura M (1980) A simple model for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  30. Kuan MG (2004) Carbon sequestration and stabilization in soils: implications for soil productivity and climate change. Soil Sci Plant Nutr 50:467–476

    Google Scholar 

  31. Lal R (2004) Soil carbon sequestration impacts on global climate change and food security. Science 304:1623–1627

    Article  CAS  PubMed  Google Scholar 

  32. Lundquist E, Jackson LE, Scow K, Hsu C (1999) Changes in microbial biomass and community composition, and soil carbon and nitrogen pools after incorporation of rye into three California agricultural soils. Soil Biol Biochem 31:221–236

    Article  CAS  Google Scholar 

  33. Moore JC, Berlow EL, Coleman DC, de Ruiter PC, Dong Q, Hastings A, Collins Johnson JC, McCann KS, Melville K, Morin PJ, Nadelhoffer K, Rosemond AD, Post DM, Sabo JL, Scow KM, Vanni MJ, Wall DH (2004) Detritus, trophic dynamics and biodiversity. Ecol Lett 7:584–600

    Article  Google Scholar 

  34. Nicolardot B, Fauvet G, Cheneby D (1994) Carbon and nitrogen cycling through soil microbial biomass at various temperatures. Soil Biol Biochem 26:253–261

    Article  CAS  Google Scholar 

  35. Nicolardot B, Recous S, Mary B (2001) Simulation of C and N mineralization during crop residue decomposition: a simple dynamic model based on the C:N ratio of the residues. Plan Soil 228:83–103

    Article  CAS  Google Scholar 

  36. Nicolardot B, Bouziri L, Bastian F, Ranjard L (2007) A microcosm experiment to evaluate the influence of the location and quality of plant residues on residue decomposition and genetic structure of soil microbial communities. Soil Biol Biochem 39:1631–1644

    Article  CAS  Google Scholar 

  37. Padmanabhan P, Padmanabhan S, DeRito C, Gray A, Gannon D, Snape JR, Tsai CS, Park W, Jeon C, Madsen EL (2003) Respiration of 13C-labeled substrates added to soil in the field and subsequent 16 rRNA gene analysis of 13C-labeled soil DNA. Appl Environ Microbiol 69:1614–1622

    Article  CAS  PubMed  Google Scholar 

  38. Pankhurst CE, Kirkby CA, Hawke BG, Harch BD (2002) Impact of a change in tillage and crop residue management practice on soil chemical and microbiological properties in a cereal-producing red duplex soil in NSW, Australia. Biol Fertil Soils 35:189–196

    Article  CAS  Google Scholar 

  39. Parr JF, Papendick RI (1978) Factors affecting the decomposition of crop residues by microorganisms. In: Oschwld WR (ed.) Crop residues management systems. ASA Spec. Publ. 31. ASA, CSSA, SSSA, Madison, WI, pp: 101–129

  40. Piccolo A (1996) Humus and soil conservation. In: Piccolo A (ed) Humic substances in terrestrial ecosystems. Elsevier, Amsterdam, pp 225–264

    Chapter  Google Scholar 

  41. Rangel-Castro JI, Prosser JI, Ostle N, Scrimgeour CM, Killham K, Meharg AA (2005) Flux and turnover of fixed carbon in soil microbial biomass of limed and unlimed plots of an upland grassland ecosystem. Environ Microbiol 7:544–552

    Article  CAS  PubMed  Google Scholar 

  42. Ranjard L, Poly F, Lata JC, Mougel C, Thioulouse J, Nazaret S (2001) Characterization of bacterial and fungal soil communities by automated ribosomal intergenic spacer analysis fingerprints: biological and methodological variability. Appl Environ Microbiol 67:4479–4487

    Article  CAS  PubMed  Google Scholar 

  43. Ranjard L, Lejon DPH, Mougel C, Schehrer L, Merdinoglu D, Chaussod R (2003) Sampling strategy in molecular ecology: influence of soil sample size on DNA fingerprinting analysis of fungal and bacterial communities. Environ Microbiol 5:1111–1120

    Article  CAS  PubMed  Google Scholar 

  44. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  45. Sarwar M, Kirkegaard JA, Wong PTW, Desmarchelier JM (1998) Biofumigation potential of brassicas—III. In vitro toxicity of isothiocyanates to soil-borne fungal pathogens. Plant Soil 201:103–112

    Article  CAS  Google Scholar 

  46. Shepherd KD, Vanlauwe B, Gachengo CN, Palm CA (2005) Decomposition and mineralization of organic residues predicted using near infrared spectroscopy. Plant Soil 277:315–333

    Article  CAS  Google Scholar 

  47. Stenberg B, Jensen LS, Nordkvist E, Breland TA, Pedersen A, Guðmundsson J, Bruun S, Salo T, Palmason F, Hendriksen TM, Korsaeth A (2004) Near infrared reflectance spectroscopy for quantification of crop residue, green manure and catch crop C and N fractions governing decomposition dynamics in soil. J Near Infrared Spectrosc 12:331–346

    Article  CAS  Google Scholar 

  48. Thioulouse J, Chessel D, Dolédec S, Oliver JM (1997) Ade-4: a multivariate analysis and graphical display software. Stat Comput 7:75–83

    Article  Google Scholar 

  49. Thompson JD, Higgins DG, Gibson TJ (1994) ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positionspecific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  50. Trinsoutrot I, Recous S, Bentz B, Lineres M, Cheneby D, Nicolardot B (2000) Biochemical quality of crop residues and carbon and nitrogen mineralization kinetics under nonlimiting nitrogen conditions. Soil Sci Soc Am J 64:918–926

    Article  CAS  Google Scholar 

  51. Vanlauwe B, Nwoke OCN, Sanginga N, Merckx R (1996) Impact of residues quality on the C and N mineralization of leaf and root residues of three agroforestry species. Plant Soil 183:221–231

    Article  CAS  Google Scholar 

  52. Barros VA, AS SA, Delgadillo I, Copikova J, Coimbra MA (2007) Infrared spectroscopy and outer product analysis for quantification of fat, nitrogen, and moisture of cocoa powder. Anal Chim Acta 601:77–86

    Article  PubMed  Google Scholar 

  53. Workman JJr, Weyer L (2008) Practical guide to interpretive near-infrared spectroscopy (CRC Press. Taylor & Francis Group, New York)

    Google Scholar 

  54. Xu JM, Tang C, Chen ZL (2006) Chemical composition controls residue decomposition in soil differing in initial pH. Soil Biol Biochem 38:544–552

    Article  CAS  Google Scholar 

Download references

Acknowledgement

This ECOGER project was supported by an ECCO grant from the French National Research Agency (ANR). N. Pascault received a grant from the Agence de l'Environnement et de la Maîtrise de l'Energie (ADEME), and the Burgundy region. The authors are grateful to the CEMAGREF of Grenoble and S. De Danieli and J.J. Brun for the NIR analysis. Thanks are also extended to C. Faivre, S. Dequiedt, and F. Bastian for their technical help.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pierre-Alain Maron.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Figure S1

Supplemental data. Loading matrices of PC1 and PC2 for principal component analysis of NIR fingerprints of all residues (a, b); wheat (c, d); rape (e, f); and alfalfa (g, h) residues. Gray gradation represents loading values from −1 (black) to +1 (white). Threshold values of −0.8 and +0.8 were used for the identification of wavebands explanatory for each principal component represented in Table 1. Wavenumbers are expressed per centimeter. (DOC 602 kb)

Figure S2

Supplemental data. Rarefaction curves for wheat, rape, and alfalfa resides at T22 and T254 day after incorporation to soil, respectively. (DOC 54 kb)

Figure S3

Supplemental data. Microbial C-biomass determined by analysis of the total soil fatty acid (PLFA) content in the soil after incorporation of wheat, rape, and alfalfa residue. (DOC 72 kb)

Figure S4

Supplemental data. Rainfall (mm) and atmospheric temperature (°C) during the experiment. (DOC 78 kb)

Table S1

Supplemental data. Closest affiliations of 16S rDNA sequences cloned from DNA extracted from wheat, rape, and alfalfa residue for July 2006 and March 2007 (22 and 254 days after incorporation, respectively). The accession numbers for the 16S rDNA gene sequences were deposited in the GeneBank database (from GQ379348 to GQ379673). (DOC 451 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pascault, N., Cécillon, L., Mathieu, O. et al. In Situ Dynamics of Microbial Communities during Decomposition of Wheat, Rape, and Alfalfa Residues. Microb Ecol 60, 816–828 (2010). https://doi.org/10.1007/s00248-010-9705-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-010-9705-7

Keywords

Navigation