Microbial Ecology

, Volume 50, Issue 1, pp 73–81 | Cite as

Competing Factors of Compost Concentration and Proximity to Root Affect the Distribution of Streptomycetes

  • Ehud Inbar
  • Stefan J. Green
  • Yitzhak Hadar
  • Dror Minz
Microbial Ecology

Abstract

Streptomycetes are important members of soil microbial communities and are particularly active in the degradation of recalcitrant macromolecules and have been implicated in biological control of plant disease. Using a streptomycetes-specific polymerase chain reaction (PCR)-denaturing gradient gel electrophoresis (PCR-DGGE) methodology coupled with band excision and sequence analysis, we examined the effect of grape marc compost amendment to soil on cucumber plant–associated streptomycetes community composition. We observed that both compost amendment and proximity to the root surface influenced the streptomycetes community composition. A strong root selection for a soil-derived Streptomycete, most closely related to Streptomycesthermotolerans, S. iakyrus, and S. thermocarboxydus, was independent of compost amendment rate. However, while the impact of compost amendment was mitigated with increasing proximity to the root, high levels of compost amendment resulted in the detection of compost-derived species on the root surface. Conversely, in rhizosphere and non-rhizosphere soils, the community composition of streptomycetes was affected strongly even by modest compost amendment. The application of a streptomycetes-specific PCR primer set combined with DGGE analysis provided a rapid means of examining the distribution and ecology of streptomycetes in soils and plant-associated environments.

References

  1. 1.
    Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefPubMedGoogle Scholar
  2. 2.
    Araragi M (1979) Comparison of actinomycete flora between tropical and temperate upland farm soils. Soil Sci Plant Nutr 25:245–254Google Scholar
  3. 3.
    Arisawa A, Tsunekawa H, Okamura K, Okamoto R (1995) Nucleotide sequence analysis of the carbomycin biosynthetic genes including the 3–O–acyltransferase gene from Streptomyces thermotolerans. Biosci Biotechnol Biochem 59:582–588PubMedGoogle Scholar
  4. 4.
    Balla P (1970) A description of thermophilic actinomycetes cultivated from champignon compost. Sect Biol 12:99–106Google Scholar
  5. 5.
    Boehm MJ, Wu TY, Stone AG, Kraakman B, Iannotti DA, Wilson GE, Madden LV, Hoitink HAJ (1997) Cross-polarized magic-angle spinning C-13 nuclear magnetic resonance spectroscopic characterization of soil organic matter relative to culturable bacterial species composition and sustained biological control of Pythium root rot. Appl Environ Microbiol 63:162–168Google Scholar
  6. 6.
    Boyle JS, Lew AM (1995) An inexpensive alternative to glassmilk for DNA purification. Trends Genet 11:8CrossRefPubMedGoogle Scholar
  7. 7.
    Challis GL, Hopwood DA (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci USA 100 (Suppl 2): 14555–14561CrossRefPubMedGoogle Scholar
  8. 8.
    Cheng W, Coleman DC, Carroll CR, Hoffman CA (1993) In situ measurement of root respiration and soluble C concentrations in the rhizosphere. Soil Biol Biochem 25:1189–1196CrossRefGoogle Scholar
  9. 9.
    Conn VM, Franco CM (2004) Analysis of the endophytic Actinobacterial population in the roots of wheat (Triticum aestivum L.) by terminal restriction fragment length polymorphism and sequencing of 16S rRNA clones. Appl Environ Microbiol 70:1787–1794CrossRefPubMedGoogle Scholar
  10. 10.
    Craft CM, Nelson EB (1996) Microbial properties of composts that suppress damping-off and root rot of creeping bentgrass caused by Pythium graminicola. Appl Environ Microbiol 62:1550–1557Google Scholar
  11. 11.
    Crawford DL, Lynch JM, Whipps JM, Ousley MA (1993) Isolation and characterization of actinomycete antagonists of a fungal root pathogen. Appl Environ Microbiol 59:3899–3905Google Scholar
  12. 12.
    de Brito Alvarez MA, Gagne S, Antoun H (1995) Effect of compost on rhizosphere microflora of the tomato and on the incidence of plant growth–promoting rhizobacteria. Appl Environ Microbiol 61:194–199Google Scholar
  13. 13.
    Dees PM, Ghiorse WC (2001) Microbial diversity in hot synthetic compost as revealed by PCR–amplified rRNA sequences from cultivated isolates and extracted DNA. FEMS Microbiol Ecol 35:207–216CrossRefPubMedGoogle Scholar
  14. 14.
    Dick WA, McCoy EL (1993) Enhancing soil fertility by addition of compost. In: Hoitink HAJ, Keener HM (Eds). Science and Engineering of Composting: Design, Environmental, Microbiological and Utilization Aspects, Renaissance Publications, Worthington, OH, pp 622–644Google Scholar
  15. 15.
    Dickinson CH, Dawson D, Goodfellow M (1981) Interactions between bacteria, streptomycetes and fungi from Picea sitchensis litter. Soil Biol Biochem 13:65–71CrossRefGoogle Scholar
  16. 16.
    Doumbou CL, Akimov V, Cote M, Charest PM, Beaulieu C (2001) Taxonomic study on nonpathogenic streptomycetes isolated from common scab lesions on potato tubers. Syst Appl Microbiol 24:451–456CrossRefPubMedGoogle Scholar
  17. 17.
    Egan S, Wiener P, Kallifidas D, Wellington EMH (2001) Phylogeny of Streptomyces species and evidence for horizontal transfer of entire and partial antibiotic gene clusters. Anton Leeuw Int J G 79:127–133Google Scholar
  18. 18.
    Green SJ, Michel FC, Jr., Hadar Y, Minz D (2004) Similarity of bacterial communities in sawdust– and straw–amended cow manure composts. FEMS Microbiol Lett 233:115–123CrossRefPubMedGoogle Scholar
  19. 19.
    Hardy GES, Sivasithamparam K (1995) Antagonism of fungi and actinomycetes isolated from composted eucalyptus bark to Phytophthora drechsleri in a steamed and nonsteamed composted eucalyptus bark-amended container medium. Soil Biol Biochem 27:243–246CrossRefGoogle Scholar
  20. 20.
    Herrmann RF, Shann JF (1997) Microbial community changes during the composting of municipal solid waste. Microb Ecol 33:78–85CrossRefPubMedGoogle Scholar
  21. 21.
    Heuer H, Krsek M, Baker P, Smalla K, Wellington EM (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63:3233–3241PubMedGoogle Scholar
  22. 22.
    Hoitink HAJ, Boehm M (1999) Biocontrol within the context of soil microbial communities: A substrate-dependent phenomenon. Annu Rev Phytopathol 37:427–446CrossRefPubMedGoogle Scholar
  23. 23.
    Katsifas EA, Koraki TG, Karagouni AD (2000) Determination of metabolic activity of streptomycetes in soil microcosms. J Appl Microbiol 89:178–184CrossRefPubMedGoogle Scholar
  24. 24.
    Kleyn JG, Wetzler TF, (1981) The microbiology of spent mushroom compost and its dust. Can J Microbiol 27:748–753PubMedGoogle Scholar
  25. 25.
    Korn-Wendisch F, Kutzner HJ (1999) The family Streptomycetaceae. In: Dworkin M (Ed). The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community, 3rd ed, Springer–Verlag, New YorkGoogle Scholar
  26. 26.
    Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (Eds) Nucleic Acid Techniques in Bacterial Systematics, John Wiley & Sons, Chichester, UK, pp 115–175Google Scholar
  27. 27.
    Langlois P, Bourassa S, Poirier GG, Beaulieu C (2003) Identification of Streptomyces coelicolor proteins that are differentially expressed in the presence of plant material. Appl Environ Microbiol 69:1884–1889CrossRefPubMedGoogle Scholar
  28. 28.
    Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371CrossRefPubMedGoogle Scholar
  29. 29.
    Miyairi K, Ogasawara A, Tonouchi A, Hosaka K, Kudou M, Okuno T (2004) Low-molecular-weight pectate lyase I from Streptomyces thermocarboxydus. J Appl Glycosci 51:1–7Google Scholar
  30. 30.
    Miyashita K, Kato T, Tsuru S (1982) Actinomycetes occurring in soil applied with compost. Soil Sci Plant Nutr 28:303–313Google Scholar
  31. 31.
    Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Anton Leeuw Int J G 73:127–141Google Scholar
  32. 32.
    Rabikowitz S., (1981) ‘The Soils of Israel: Creation, Nature and Characteristics”[Hebrew]. Kibbutz Hameuchad Publishing House, Tel Aviv, 489 pGoogle Scholar
  33. 33.
    Rintala H, Nevalainen A, Ronka E, Suutari M (2001) PCR primers targeting the 16S rRNA gene for the specific detection of Streptomycetes. Mol Cell Probes 15:337–347CrossRefPubMedGoogle Scholar
  34. 34.
    Rothrock CS, Gottlieb D (1984) Role of antibiosis in antagonism of Streptomyces hygroscopicus var geldanus to Rhizoctonia solani in Soil. Can J Microbiol 30:1440–1447Google Scholar
  35. 35.
    Ryckeboer J, Mergaert J, Coosemans J, Deprins K, Swings J (2003) Microbiological aspects of biowaste during composting in a monitored compost bin. J Appl Microbiol 94:127–137CrossRefPubMedGoogle Scholar
  36. 36.
    Semenov AM, van Bruggen AHC, Zelenev VV (1999) Moving waves of bacterial populations and total organic carbon along roots of wheat. Microb Ecol 37:116–128CrossRefPubMedGoogle Scholar
  37. 37.
    Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751CrossRefPubMedGoogle Scholar
  38. 38.
    Song J, Weon HY, Yoon SH, Park DS, Go SJ, Suh JW (2001) Phylogenetic diversity of thermophilic actinomycetes and Thermoactinomyces spp. isolated from mushroom composts in Korea based on 16S rRNA gene sequence analysis. FEMS Microbiol Lett 202:97–102CrossRefPubMedGoogle Scholar
  39. 39.
    Stach JE, Maldonado LA, Ward AC, Goodfellow M, Bull AT (2003) New primers for the class Actinobacteria: application to marine and terrestrial environments. Environ Microbiol 5:828–841CrossRefPubMedGoogle Scholar
  40. 40.
    Takeuchi T, Sawada H, Tanaka F, Matsuda I (1996) Phylogenetic analysis of Streptomyces spp. causing potato scab based on 16S rRNA sequences. Int J Syst Bacteriol 46:476–479PubMedGoogle Scholar
  41. 41.
    Thirup L, Johnsen K, Winding A (2001) Succession of indigenous Pseudomonas spp. and actinomycetes on barley roots affected by the antagonistic strain Pseudomonas fluorescens DR54 and the fungicide imazalil. Appl Environ Microbiol 67:1147–1153CrossRefPubMedGoogle Scholar
  42. 42.
    Tiquia SM, Wan JHC, Tam NFY (2002) Microbial population dynamics and enzyme activities during composting. Compost Sci Util 10:150–161Google Scholar
  43. 43.
    Tokala RK, Strap JL, Jung CM, Crawford DL, Salove MH, Deobald LA, Bailey JF, Morra MJ (2002) Novel plant–microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl Environ Microbiol 68:2161–2171CrossRefPubMedGoogle Scholar
  44. 44.
    van Overbeek LS, Cassidy M, Kozdroj J, Trevors JT, van Elsas JD (2002) A polyphasic approach for studying the interaction between Ralstonia solanacearum and potential control agents in the tomato phytosphere. J Microbiol Meth 48:69–86CrossRefGoogle Scholar
  45. 45.
    Weller DM, Raaijmakers JM, Gardener BB, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348PubMedGoogle Scholar
  46. 46.
    Whipps JM (1990) Carbon economy. In: Lynch JM (Ed). The Rhizosphere, John Wiley & Sons, New York, pp 59–97Google Scholar
  47. 47.
    Wieland G, Neumann R, Backhaus H (2001) Variation of microbial communities in soil, rhizosphere, and rhizoplane in response to crop species, soil type, and crop development. Appl Environ Microbiol 67:5849–5854CrossRefPubMedGoogle Scholar
  48. 48.
    You MP, Sivasithamparam K (1995) Changes in microbial-populations of an avocado plantation mulch suppressive of Phytophthora cinnamomi. Appl Soil Ecol 2:33–43CrossRefGoogle Scholar
  49. 49.
    Yuan WM, Crawford DL (1995) Characterization of Streptomyces lydicus WYEC 108 as a potential biocontrol agent against fungal root and seed rots. Appl Environ Microbiol 61:3119–3128PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • Ehud Inbar
    • 1
    • 2
  • Stefan J. Green
    • 1
    • 2
  • Yitzhak Hadar
    • 1
  • Dror Minz
    • 2
  1. 1.Faculty of Agricultural, Food and Environmental Quality SciencesHebrew University of JerusalemIsrael
  2. 2.Institute of Soil, Water and Environmental SciencesAgricultural Research Organization, The Volcani CenterIsrael

Personalised recommendations