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Microbial Ecology

, Volume 76, Issue 1, pp 169–181 | Cite as

Bacterial Shifts in Nutrient Solutions Flowing Through Biofilters Used in Tomato Soilless Culture

  • David Renault
  • Franck Déniel
  • Jessica Vallance
  • Emilie Bruez
  • Jean-Jacques Godon
  • Patrice Rey
Environmental Microbiology

Abstract

In soilless culture, slow filtration is used to eliminate plant pathogenic microorganisms from nutrient solutions. The present study focused on the characterization and the potential functions of microbial communities colonizing the nutrient solutions recycled on slow filters during a whole cultivation season of 7 months in a tomato growing system. Bacterial microflora colonizing the solutions before and after they flew through the columns were studied. Two filters were amended with Pseudomonas putida (P-filter) or Bacillus cereus strains (B-filter), and a third filter was a control (C-filter). Biological activation of filter unit through bacterial amendment enhanced very significantly filter efficacy against plant potential pathogens Pythium spp. and Fusarium oxysporum. However, numerous bacteria (103–104 CFU/mL) were detected in the effluent solutions. The community-level physiological profiling indicated a temporal shift of bacterial microflora, and the metabolism of nutrient solutions originally oriented towards carbohydrates progressively shifted towards degradation of amino acids and carboxylic acids over the 7-month period of experiment. Single-strand conformation polymorphism fingerprinting profiles showed that a shift between bacterial communities colonizing influent and effluent solutions of slow filters occurred. In comparison with influent, 16S rDNA sequencing revealed that phylotype diversity was low in the effluent of P- and C-filters, but no reduction was observed in the effluent of the B-filter. Suppressive potential of solutions filtered on a natural filter (C-filter), where the proportion of Proteobacteria (α- and β-) increased, whereas the proportion of uncultured candidate phyla rose in P- and B-filters, is discussed.

Keywords

Bacterial communities Soilless culture Recirculating solutions Single-strand conformation polymorphism Community level physiological profiling 

Notes

Acknowledgements

This project was supported by the Regional Councils of Brittany and Pays de la Loire and by the French Ministry of Research.

Supplementary material

248_2017_1117_MOESM1_ESM.docx (173 kb)
Supplementary Table 1 Abundance of 16S–ribosomal RNA gene phylotypes in the clone libraries constructed from nutrient solutions sampled from influent and effluent of C-filter (iClib, eClib), B-filter (iBlib, eBlib) and P-filter (iPlib, ePlib). For each phylotype affiliation, the closest described relative from the GenBank database with its accession number (in brackets) and the percentage of similarity as given by the Blast program are provided. (DOCX 172 kb)

References

  1. 1.
    Stanghellini ME, Rasmussen SL (1994) Hydroponics, a solution for zoosporic pathogens. Plant Dis. 78:1129–1138CrossRefGoogle Scholar
  2. 2.
    Vallance J, Déniel F, Le Floch G, Guérin-Dubrana L, Blancard D, Rey P (2011) Potentially pathogenic and beneficial microorganisms in soilless cultures. A review. Agron. Sustain. Dev. 31:191–203CrossRefGoogle Scholar
  3. 3.
    Davies JML (1980) Diseases in NFT. Acta Hort 98:299–305CrossRefGoogle Scholar
  4. 4.
    Evans SG (1979) Susceptibility of plants to fungal pathogens when grown by the nutrient-film technique (NFT). Plant Pathol. 28:45–48CrossRefGoogle Scholar
  5. 5.
    Runia WT (1995) A review of possibilities for disinfection of recirculation water from soilless cultures. Acta Hort 382:221–229CrossRefGoogle Scholar
  6. 6.
    Paulitz TC (1997) Biological control of root pathogens in soilless and hydroponic systems. Hortscience 32:193–196Google Scholar
  7. 7.
    McPherson GM, Harriman MR, Pattison D (1995) The potential for spread of root diseases in recirculating hydroponic systems and their control with disinfection. Meded Fac Landbouwwet Univ Gent 60/2b:371–379Google Scholar
  8. 8.
    Van OEA (1999) Closed soilless growing systems: a sustainable solution for Dutch greenhouse horticulture. Water Sci. Technol. 39:105–112CrossRefGoogle Scholar
  9. 9.
    Ehret DL, Alsanius B, Wohanka W, Menzies JG, Utkhede R (2001) Disinfestation of recirculating nutrient solutions in greenhouse horticulture. Agronomie 21:323–339CrossRefGoogle Scholar
  10. 10.
    Postma J, Willemsen de Klein MJEIM, van Elsas FD (2000) Effect of the indigenous microflora on the development of root and crown rot caused by Pythium aphanidermatum in cucumber grown on rockwool. Phytopathology 90:125–133CrossRefPubMedGoogle Scholar
  11. 11.
    Zhang W, JC T (2000) Effect of ultraviolet disinfection of hydroponic solutions on Pythium root rot and non-target bacteria. Eur. J. Plant Pathol. 106:415–421CrossRefGoogle Scholar
  12. 12.
    Tu JC, Papadopoulos AP, Hao X, Zheng J (1999) The relationship of Pythium root rot and rhizosphere microorganisms in a closed circulating and an open system in rockwool culture of tomato. Acta Hort 481:577–583CrossRefGoogle Scholar
  13. 13.
    Chave M, Dabert P, Brun R, Godon JJ, Poncet C (2008) Dynamics of rhizoplane bacterial communities subjected to physicochemical treatments in hydroponic crops. Crop Prot. 27:418–426CrossRefGoogle Scholar
  14. 14.
    Postma J, Geraats BPJ, Pastoor R, van Elsas JD (2005) Characterization of the microbial community involved in the suppression of Pythium aphanidermatum in cucumber grown on rockwool. Phytopathology 95:808–818CrossRefPubMedGoogle Scholar
  15. 15.
    Ellis KV (1985) Slow sand filtration. Crit Rev Environ Contr 15:315–354CrossRefGoogle Scholar
  16. 16.
    Wohanka W (1995) Disinfection of recirculating nutrient solutions by slow sand filtration. Acta Hort 382:246–255CrossRefGoogle Scholar
  17. 17.
    Rey P, Picard K, Déniel F, Benhamou N, Tirilly Y (1999) Development of an IPM sytem in soilless culture by using slow sand filtration and a biocontrol fungus, Pythium oligandrum. IOBC Bulletin 22:205–208Google Scholar
  18. 18.
    Van OEA, Amsing JJ, van Kuik AJ, Willers H (1999) Slow filtration: a potential method for the elimination of pathogens and nematodes in recirculating nutrient solutions from glasshouse-grown crops. Acta Hort 481:519–526CrossRefGoogle Scholar
  19. 19.
    Brand T, Wohanka W (2001) Importance and characterization of the biological component in slow filters. Acta Hort 554:313–321CrossRefGoogle Scholar
  20. 20.
    Calvo-Bado LA, Pettitt TR, Parsons N, Petch GM, Morgan JAW, Whipps JM (2003) Spatial and temporal analysis of the microbial community in slow sand filters used for treating horticultural irrigation water. Appl. Environ. Microbiol. 69:2116–2125CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Renault D, Tirilly Y, Benizri E, Sohier D, Barbier G, Rey P (2007) Characterization of Bacillus and Pseudomonas strains with suppressive traits isolated from tomato hydroponic-slow filtration unit. Can. J. Microbiol. 53:784–797CrossRefPubMedGoogle Scholar
  22. 22.
    Déniel F, Rey P, Chérif M, Guillou A, Tirilly Y (2004) Indigenous bacteria with antagonistic and plant-growth-promoting activities improve slow-filtration efficiency in soilless cultivation. Can. J. Microbiol. 50:499–508CrossRefPubMedGoogle Scholar
  23. 23.
    Déniel F, Renault D, Tirilly Y, Barbier RP (2006) Dynamic filtration in tomato soilless greenhouse: evolution of microbial communities on filtering media and control of potentially suppressive and pathogenic microorganisms. Agron. Sustain. Dev. 26:185–193CrossRefGoogle Scholar
  24. 24.
    Berkelmann B, Wohanka W, Wolf GA (1994) Characterization of the bacterial flora in circulating nutrient solutions of a hydroponic system with rockwool. Acta Hort 361:372–381CrossRefGoogle Scholar
  25. 25.
    Koohakan P, Ikeda H, Jeanaksorn T, Tojo M, Kusakari SI, Okada K, Sato S (2004) Evaluation of the indigenous microorganisms in soilless culture: occurrence and quantitative characteristics in the different growing systems. Sci. Hortic. 101:179–188CrossRefGoogle Scholar
  26. 26.
    Van OEA, Postma J (2000) Prevention of root diseases in closed soilless growing systems by microbial optimisation and slow sand filtration. Acta Hort 532:97–102CrossRefGoogle Scholar
  27. 27.
    Renault D, Vallance J, Déniel F, Wery N, Godon JJ, Barbier G, Rey P (2012) Diversity of bacterial communities that colonize the filter units used for controlling plant pathogens in soilless cultures. Microb Ecol 63:170–187CrossRefPubMedGoogle Scholar
  28. 28.
    Jeffers SN, Martin SB (1986) Comparison of two media selective for Phytophthora and Pythium species. Plant Dis. 70:1038–1043CrossRefGoogle Scholar
  29. 29.
    Komada H (1975) Development of a selective medium for quantitative isolation of Fusarium oxysporum from natural soils. Rev Plant Prot Res 8:114–125Google Scholar
  30. 30.
    Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl. Environ. Microbiol. 57:2351–2359PubMedPubMedCentralGoogle Scholar
  31. 31.
    Garland JL (1996) Analytical approaches to the characterization of samples of microbial communities using patterns of potential C source utilization. Soil Biol. Biochem. 28:213–221CrossRefGoogle Scholar
  32. 32.
    Grove JA, Kautola H, Javadpour S, Moo-Young M, Anderson WA (2004) Assessment of changes in the microorganism community in a biofilter. Biochem. Eng. J. 18:111–114CrossRefGoogle Scholar
  33. 33.
    Godon JJ, Zumstein E, Dabert P, Habouzit F, Moletta R (1997) Molecular microbial diversity of an anaerobic digestor as determined by small-subunit rDNA sequence analysis. Appl. Environ. Microbiol. 63:2802–2813PubMedPubMedCentralGoogle Scholar
  34. 34.
    Zemb O, Haegeman B, Delgenes JP, Lebaron P, Godon JJ (2007) SAFUM: statistical analysis of SSCP fingerprints using PCA projections, dendrograms and diversity estimators. Mol. Ecol. Notes 7:767–770CrossRefGoogle Scholar
  35. 35.
    Fox J (2005) The R Commander: a basic statistics graphical user interface to R. J Stat Softw 14(9):1–42CrossRefGoogle Scholar
  36. 36.
    Ewing B, Hillier L, Wendl M, Green P (1998) Basecalling of automated sequencer traces using phred. Genome Res. 8:175–194CrossRefPubMedGoogle Scholar
  37. 37.
    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J. Mol. Biol. 215:403–410CrossRefPubMedGoogle Scholar
  38. 38.
    Yarza P, Richter M, Peplies J, Euzeby J, Amann R, Schleifer KH, Ludwig W, Glöckner FO, Roselló-Móra R (2008) The all-species living tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst. Appl. Microbiol. 31:241–250CrossRefPubMedGoogle Scholar
  39. 39.
    Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264CrossRefGoogle Scholar
  40. 40.
    Colwell RK (2005) EstimateS version 7.5: statistical estimation of species richness and shared species from samples; user’s guide and application published at http://purl.oclc.org/estimates
  41. 41.
    Chao A, Chazdon RL, Colwell RK, Shen TJ (2005) A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol. Lett. 8:148–159CrossRefGoogle Scholar
  42. 42.
    Rappé MS, Giovannoni SJ (2003) The uncultured microbial majority. Ann Rev Microbiol 57:369–394CrossRefGoogle Scholar
  43. 43.
    Harris JK, Kelley ST, Pace NR (2004) New perspective on uncultured bacterial phylogenetic division OP11. Appl. Environ. Microbiol. 70:845–849CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng JF, Darling A, Malfatti S, Swan BK, Gies EA, Dodsworth JA, Hedlund BP, Tsiamis G, Sievert SM, Liu WT, Eisen JA, Hallam SJ, Kyrpides NC, Stepanauskas R, Rubin EM, Hugenholtz P, Woyke T (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature 499:431–437CrossRefPubMedGoogle Scholar
  45. 45.
    Ferrari B, Winsley T, Ji M, Neilan B (2014) Insights into the distribution and abundance of the ubiquitous Candidatus Saccharibacteria phylum following tag pyrosequencing. Sci. Rep. 4(3957):1–9Google Scholar
  46. 46.
    Yeoh YK, Sekiguchi Y, Parks DH, Hugenholtz P (2015) Comparative genomics of candidate phylum TM6 suggests that parasitism is widespread and ancestral in this lineage. Mol Biol Evol 33:915–927Google Scholar
  47. 47.
    Oyaizu H, Matsumoto S, Minamisawa K, Gamou T (1993) Distribution of rhizobia in leguminous plants surveyed by phylogenetic identification. J. Gen. Appl. Microbiol. 39:339–354CrossRefGoogle Scholar
  48. 48.
    Gao J, Terefework Z, Chen W, Lindström K (2001) Genetic diversity of rhizobia from Astragalus adsurgens growing in different geographical regions of China. J. Biotechnol. 91:155–168CrossRefPubMedGoogle Scholar
  49. 49.
    Ogita N, Hashidoko Y, Limin SH, Tahara S (2006) Linear 3-hydroxybutyrate tetramer (HB4) produced by Sphingomonas sp. is characterized as a growth promoting factor for some rhizomicrofloral composers. Biosci. Biotechnol. Biochem. 70(9):2325–2329CrossRefPubMedGoogle Scholar
  50. 50.
    Steinberg C, Moulin F, Gaillard P, Gautheron N, Stawiecki K, Bremeersch P, Alabouvette C (1994) Disinfection of drain water in greenhouses using a wet condensation heater. Agronomie 14:627–635CrossRefGoogle Scholar
  51. 51.
    Rey P, Déniel F, Vasseur V, Benhamou N, Tirilly Y (2001) Evolution of Pythium spp. populations in soilless cultures and their control by active disinfecting methods. Acta Hort 554:341–348CrossRefGoogle Scholar
  52. 52.
    Calvo-Bado LA, Petch G, Parsons NR, Morgan JAW, Pettitt TR, Whipps JM (2006) Microbial community responses associated with the development of oomycete plant pathogens on tomato roots in soilless growing systems. J. Appl. Microbiol. 100:1194–1207CrossRefPubMedGoogle Scholar
  53. 53.
    Campbell CD, Grayston SJ, Hirst DJ (1997) Use of rhizosphere carbon sources in sole carbon source tests to discriminate soil microbial communities. J. Microbiol. Methods 30:33–41CrossRefGoogle Scholar
  54. 54.
    Benizri E, Dedourge O, Dibattista-Leboeuf C, Piutti S, Nguyen C, Guckert A (2002) Effect of maize rhizodeposits on soil microbial community structure. Appl. Soil Ecol. 21:261–265CrossRefGoogle Scholar
  55. 55.
    Alsanius BW, Khalil S, Hultberg M (1998) Biochemical and chemical characterization of Pythium ultimum. Meded Fac Landbouwwet Univ Gent 63/3a:891–897Google Scholar
  56. 56.
    Vallance J, Déniel F, Barbier G, Guérin-Dubrana L, Benhamou N, Rey P (2012) Influence of Pythium oligandrum on the bacterial communities that colonize the nutrient solutions and the rhizosphere of tomato plants. Can. J. Microbiol. 58:1124–1134CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  • David Renault
    • 1
    • 2
  • Franck Déniel
    • 3
  • Jessica Vallance
    • 1
    • 2
  • Emilie Bruez
    • 2
  • Jean-Jacques Godon
    • 4
  • Patrice Rey
    • 1
    • 2
  1. 1.Bordeaux Sciences Agro, UMR1065 Santé et Agroécologie du Vignoble (SAVE), ISVVUniversité de BordeauxVillenave d’OrnonFrance
  2. 2.INRA, UMR1065 SAVE, ISVVVillenave d’OrnonFrance
  3. 3.Université de Bretagne Occidentale, EA 3882, Laboratoire Universitaire de Biodiversité et Ecologie MicrobienneIBSAM, ESIAB, Technopôle Brest-IroisePlouzanéFrance
  4. 4.Laboratoire de Biotechnologie de l’Environnement, INRANarbonneFrance

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