BioControl

, Volume 60, Issue 5, pp 681–689 | Cite as

Impact of temperature on the survival and the biocontrol efficacy of Lysobacter capsici AZ78 against Phytophthora infestans

  • Gerardo Puopolo
  • Maria Cristina Palmieri
  • Oscar Giovannini
  • Ilaria Pertot
Article

Abstract

Temperature can strongly influence the biocontrol efficacy of Lysobacter strains when used against phytopathogens. We investigated the influence of temperature on physiological characteristics of Lysobacter capsici AZ78 in a biocontrol situation. L. capsici AZ78 effectively colonized tomato leaves at 15 and 25 °C while exposure to 35 and 37 °C was highly detrimental. Accordingly, Phytophthora infestans attacks on tomato leaves were controlled when L. capsici AZ78 was pre-exposed to 15 and 25 °C for 24 h. Conversely, exposure to 35 °C drastically reduced the biocontrol efficacy of L. capsici AZ78 probably by impairing anti-oomycete and proteolytic activity. Furthermore, the exposure to 15 °C made the L. capsici AZ78 cells more resistant to UV light and copper ions compared to 25 and 35 °C. These findings give an indication on the best temperature range for the future use of biofungicides based on L. capsici AZ78 cells.

Keywords

Biological control Temperature Lysobacter capsici Phytophthora infestans 

Notes

Acknowledgments

The authors wish to thank Denise Ress for her technical assistance and Dr. Valerio Mazzoni for discussion on statistical analysis. This research was supported by the EU project CO-FREE (theme KBBE.2011.1.2-06, Grant agreement number 289497).

Supplementary material

10526_2015_9672_MOESM1_ESM.docx (175 kb)
Fig. S1 Effect of temperature on in vitro growth of Lysobacter capsici AZ78 in liquid medium. AZ78 cell growth was monitored over 144 h by measuring optical density at 600 nm (OD600nm) spectrophotometrically. Points indicate mean ± SE (n = 6). Supplementary material 1 (DOCX 174 kb)
10526_2015_9672_MOESM2_ESM.docx (15 kb)
Table S1 Presence of viable Lysobacter capsici AZ78 cells on the leaves of tomato plants exposed to different temperatures. Colonisation of tomato leaves by AZ78 was monitored one day (T1) and eight days (T2) after its application. AZ78 populations are expressed as log10 CFU g−1 of leaf. Values (mean values ± SE, n = 12) with different letters are significantly different between treatments according to Tukey’s test (P < 0.05). Supplementary material 2 (DOCX 15 kb)

References

  1. Baldry MGC, Dean ACR (1981) Environmental change and copper uptake by Bacillus subtilis subsp. niger and by Pseudomonas fluorescens. Biotechnol Lett 3:142–147CrossRefGoogle Scholar
  2. Bashan Y, Holguin G (1997) Azospirillum-plant relationships: environmental and physiological advances (1990–1996). Can J Microbiol 43:103–121CrossRefGoogle Scholar
  3. Burger M, Woods RG, McCarthy C, Beachman IR (2000) Temperature regulation of protease in Pseudomonas fluorescens LS107d2 by an ECF sigma factor and a transmembrane activator. Microbiology 12:3149–3155CrossRefGoogle Scholar
  4. Christensen P, Cook FD (1978) Lysobacter, a new genus of nonfruiting, gliding bacteria with a high base ratio. Int J Syst Bacteriol 28:367–393CrossRefGoogle Scholar
  5. Compant S, van der Heijden MGA, Sessitsch A (2010) Climate change effects on beneficial plant-microrganism interactions. Environ Microbiol 73:197–214Google Scholar
  6. Dé E, Orange N, Saint N, Guérillon J, De Mot R, Molle G (1997) Growth temperature dependence of channel size of the major outer-membrane protein (OprF) in psychrotrophic Pseudomonas fluorescens strains. Microbiology 143:1029–1035CrossRefPubMedGoogle Scholar
  7. Duffy BK, Défago G (1999) Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl Environ Microbiol 65:2429–2438PubMedPubMedCentralGoogle Scholar
  8. Egamberdiyeva D, Hoeflich G (2003) Influence of growth promoting bacteria on the growth of wheat in different soils and temperatures. Soil Biol Biochem 35:973–978CrossRefGoogle Scholar
  9. Elad Y, Pertot I (2012) Climate change impact on plant pathogens and plant disease. In: Manjit S. Kang (ed) Combating climate change: an agricultural perspective, CRC Press (Taylor & Francis Group), Boca Raton, FL, 183–212Google Scholar
  10. Folman LB, Postma J, van Veen JA (2003) Characterization of Lysobacter enzymogenes (Christensen and Cook 1978) strain 3.1T8, a powerful antagonist of fungal diseases of cucumber. Microbiol Res 158:107–115CrossRefPubMedGoogle Scholar
  11. Folman LB, De Klein MJEM, Postma J, van Veen JA (2004) Production of antifungal compounds by Lysobacter enzymogenes strain 3.1T8 under different conditions in relation to its efficacy as a biocontrol agent of Pythium aphanidermatum in cucumber. Biol Control 31:145–154CrossRefGoogle Scholar
  12. Franks F, Mathias SF, Hatley RH (1990) Water, temperature and life. Philos Trans R Soc Lond B Biol Sci 326:517–531CrossRefPubMedGoogle Scholar
  13. Garibaldi JA (1971) Influence of temperature on the iron metabolism of a fluorescent pseudomonad. J Bacteriol 105:1036–1038PubMedPubMedCentralGoogle Scholar
  14. Gayán E, Mañas P, Álvarez I, Condón S (2013) Mechanism of the synergistic inactivation of Escherichia coli by UV-C light at mild temperatures. Appl Environ Microbiol 79:4465–4473CrossRefPubMedPubMedCentralGoogle Scholar
  15. Geveke DJ (2008) UV inactivation of E. coli in liquid egg white. Food Bioprocess Technol 1:201–206CrossRefGoogle Scholar
  16. Hayward AC, Fegan N, Fegan M, Stirling GR (2010) Stenotrophomonas and Lysobacter: ubiquitous plant-associated gamma-proteobacteria of developing significance in applied microbiology. J App Microbiol 108:756–770CrossRefGoogle Scholar
  17. Ingraham J (1987) Effect of temperature, pH, water activity, and pressure on growth. In: Neidhardt FC, Ingraham JL, Low KB, Magasanik B, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella: cellular and molecular biology. American Society for Microbiology, Washington, DC, pp 1543–1554Google Scholar
  18. IPCC-Intergovernmental Panel on Climate Change (2014) Cimate Change. Fifth assessment synthesis report. Summary for policy makers. Available at http://www.ipcc.ch
  19. Ko H-S, Jin R-D, Krishnan HB, Lee SB, Kim K-Y (2009) Biocontrol ability of Lysobacter antibioticus HS124 against Phytophthora blight is mediated by the production of 4-hydroxyphenylacetic acid and several lytic enzymes. Curr Microbiol 59:608–615CrossRefPubMedGoogle Scholar
  20. Köhl J, Postma J, Nicot P, Ruocco M, Blum B (2011) Stepwise screening of microorganisms for commercial use in biological control of plant-pathogenic fungi and bacteria. Biol Control 57:1–12CrossRefGoogle Scholar
  21. Landa BB, Navas-Cortés RM, Jiménez-Díaz RM (2004) Influence of temperature on plant-rhizobacteria interactions related to biocontrol potential for suppression of fusarium wilt of chickpea. Plant Pathol 53:341–352CrossRefGoogle Scholar
  22. Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333:616–620CrossRefPubMedGoogle Scholar
  23. McElhaney RN (1982) Effects of membrane lipids on transport and enzymatic activities. Curr Topics Membr Transp 17:317–380CrossRefGoogle Scholar
  24. McKellar RC, Cholette H (1987) Effect of temperature shifts on extracellular proteinase-specific mRNA pools in Pseudomonas fluorescens B52. Appl Environ Microbiol 53:1973–1976PubMedPubMedCentralGoogle Scholar
  25. Nedwell DB (1999) Effect of low temperature on microbial growth: lowered affinity for substrates limits growth at low temperature. FEMS Microbiol Ecol 30:101–111CrossRefPubMedGoogle Scholar
  26. Nicot PC, Alabouvette C, Bardin M, Blum B, Kohl J, Ruocco M (2012) Review of factors influencing the success or failure of biocontrol: technical, industrial and socio-economic perspectives. IOBC/WPRS Bull 78:95–98Google Scholar
  27. Özcengiz G, Alaeddinoglu NG (1991) Bacilysin production by Bacillus subtilis: effects of bacilysin, pH and temperature. Folia Microbiol 36:522–526CrossRefGoogle Scholar
  28. Pertot I, Puopolo G, Hosni T, Pedrotti L, Jourdan E, Ongena M (2013) Limited impact of abiotic stress on surfactin production in planta and on disease resistance induced by Bacillus amyloliquefaciens S499 in tomato and bean. FEMS Microbiol Ecol 86:505–519CrossRefPubMedGoogle Scholar
  29. Pujol M, Badosa E, Montesinos E (2007) Epiphytic fitness of a biological control agent of fire blight in apple and pear orchads under Mediterranean weather conditions. FEMS Microbiol Ecol 59:186–193CrossRefPubMedGoogle Scholar
  30. Puopolo G, Giovannini O, Pertot I (2014a) Lysobacter capsici AZ78 can be combined with copper to effectively control Plasmopara viticola on grapevine. Microbiol Res 169:633–642CrossRefPubMedGoogle Scholar
  31. Puopolo G, Cimmino A, Palmieri MC, Giovannini O, Evidente A, Pertot I (2014b) Lysobacter capsici AZ78 produces cyclo(L-Pro- L-Tyr), a 2,5-diketopiperazine with toxic activity against sporangia of Phytophthora infestans and Plasmopara viticola. J Appl Microbiol 117:1168–1180CrossRefPubMedGoogle Scholar
  32. Puopolo G, Sonego P, Engelen K, Pertot I (2014c) Draft genome sequence of Lysobacter capsici AZ78, a bacterium antagonistic to plant-pathogenic oomycetes. Genome Announc 2:e00325-14CrossRefPubMedPubMedCentralGoogle Scholar
  33. Rensing C, Grass G (2003) Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27:197–213CrossRefPubMedGoogle Scholar
  34. Schmidt CS, Agostini F, Leifert C, Killham K, Mullins CE (2004) Influence of soil temperature and matric potential on sugar beet seedling colonization and suppression of Pythium damping-off by the antagonistic bacteria Pseudomonas fluorescens and Bacillus subtilis. Phytopathology 94:351–363CrossRefPubMedGoogle Scholar
  35. Sinensky M (1974) Homeoviscous adaptation: a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proc Natl Acad Sci USA 71:522–525CrossRefPubMedPubMedCentralGoogle Scholar
  36. Zhang Z, Yuen GY (2000) The role of chitinase production by Stenotrophomonas maltophilia strain C3 in biological control of Bipolaris sorokiniana. Phytopathology 90:384–389CrossRefPubMedGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2015

Authors and Affiliations

  1. 1.Department of Sustainable Agro-Ecosystems and Bioresources, Research and Innovation CentreFondazione Edmund Mach (FEM)S. Michele all’AdigeItaly

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