Persistence of a biocontrol Pseudomonas inoculant as high populations of culturable and non-culturable cells in 200-cm-deep soil profiles

Soil Biology and Biochemistry

Volumn 44, Issue 1, 2012, Pages 122-129

  Troxler, Josef ^a   Svercel, Miroslav ^a,b   Natsch, Andreas ^a   Zala, Marcello ^a   Keel, Christoph ^c   Moënne Loccoz, Yvan ^d,e,f   Défago, Geneviève ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d UNIVERSITÉ DE LYON   (France)

^e UNIVERSITÉ LYON 1   (France)

^f University of Lyon   (France)

Author keywords

Earthworms; Immunofluorescence; Pseudomonas; Soil inoculant; Soil profiles; Survival; VBNC bacteria

Indexed keywords

EARTHWORMS; IMMUNOFLUORESCENCE; PSEUDOMONAS; SOIL PROFILES; SURVIVAL;

AGRICULTURAL MACHINERY; BACTERIA; BIOCONTROL; BIOREMEDIATION; CELLS; ECOSYSTEMS; FLUORESCENCE; PHYSIOLOGY;

SOILS;

BACTERIUM; BIOCONTROL AGENT; BIOFERTILIZER; BIOREMEDIATION; CELL ORGANELLE; DEVELOPMENTAL BIOLOGY; EARTHWORM; FLUORESCENCE; HABITAT TYPE; HERB; INOCULATION; PATHOGENICITY; POPULATION STRUCTURE; RHIZOSPHERE; SOIL DEPTH; SOIL MICROORGANISM; SOIL PROFILE; SURFICIAL SEDIMENT; SURVIVAL;

BACTERIA (MICROORGANISMS); MEDICAGO SATIVA; PSEUDOMONAS; PSEUDOMONAS FLUORESCENS;

EID: 80054117478     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2011.09.020     Document Type: Article

References (61)

1. Akiew E., Trevorrow P.R. Management of bacterial wilt of tobacco. Bacterial Wilt: The Disease and its Causative Agent, Pseudomonas solanacearum 1994, 179-198. CAB International, Wallingford, Oxon UK. A.C. Hayward, G.L. Hartman (Eds.).
2. Arana I., Muela A., Orruño M., Seco C., Garaizabal I., Barcina I. Effect of temperature and starvation upon survival strategies of Pseudomonas fluorescens CHA0: comparison with Escherichia coli. FEMS Microbiology Ecology 2010, 74:500-509.
3. Binnerup S.J., Sørensen J. Long-term oxidant deficiency in Pseudomonas aeruginosa PAO303 results in cells which are nonculturable under aerobic conditions. FEMS Microbiology Ecology 1993, 13:79-84.
4. Binnerup S.J., Jensen D.F., Thordal-Christensen H., Sørensen J. Detection of viable, but nonculturable Pseudomonas fluorescens DF57 in soil using a microcolony epifluorescence technique. FEMS Microbiology Ecology 1993, 12:97-105.
5. Buck A., Oliver J.D. Survival of spinach-associated Helicobacter pylori in the viable but nonculturable state. Food Control 2010, 21:1150-1154.
6. Burke D.W. Root growth obstruction and Fusarium root rot of beans. Phytopathology 1968, 58:1575-1576.
7. Chapon A., Boutin M., Rimé D., Delalande L., Guillerm A.Y., Sarniguet A. Direct and specific assessment of colonisation of wheat rhizoplane by Pseudomonas fluorescens Pf29A. European Journal of Plant Pathology 2003, 109:61-70.
8. de Werra P., Huser A., Tabacchi R., Keel C., Maurhofer M. Plant- and microbe-derived compounds affect the expression of genes encoding antifungal compounds in a pseudomonad with biocontrol activity. Applied and Environmental Microbiology 2011, 77:2807-2812.
9. Doube B.M., Stephens P.M., Davoren C.W., Ryder M.H. Interaction between earthworms, beneficial soil microorganisms and root pathogens. Applied Soil Ecology 1994, 1:3-10.
10. Du M., Chen J.X., Zhang X.H., Li A.J., Li Y. Characterization and resuscitation of viable but nonculturable Vibrio alginolyticus VIB283. Archives of Microbiology 2007, 188:283-288.
11. Fischer S.E., Jofre E.C., Cordero P.V., Manero F.J.G., Mori G.B. Survival of native Pseudomonas in soil and wheat rhizosphere and antagonist activity against plant pathogenic fungi. Antonie Van Leeuwenhoek 2010, 97:241-251.
12. Fliessbach A., Winkler M., Lutz M.P., Oberholzer H.R., Mader P. Soil amendment with Pseudomonas fluorescens CHA0: lasting effects on soil biological properties in soils low in microbial biomass and activity. Microbial Ecology 2009, 57:611-623.
13. Flury M., Flühler H., Jury W.A., Leuenberger J. Susceptibility of soils to preferential flow of water: a field study. Water Resources Research 1994, 30:1945-1954.
14. Fontes D., Mills A.L., Hornberger G.M., Herman J.S. Physical and chemical factors influencing transport of microorganisms through porous media. Applied and Environmental Microbiology 1991, 57:2473-2481.
15. Gamalero E., Lingua G., Berta G., Lemanceau P. Methods for studying root colonization by introduced beneficial bacteria. Sustainable Agriculture 2009, 5:601-615.
16. Gannon J.T., Manilal V.B., Alexander M. Relationship between cell surface properties and transport of bacteria through soil. Applied and Environmental Microbiology 1991, 57:190-193.
17. Görres J.H., Savin M.C., Neher D.A., Weicht T.R., Amador J.A. Grazing in a porous environment: 1. The effect of soil pore structure on C and N mineralization. Plant and Soil 1999, 212:75-83.
18. Gorshkov V.Y., Petrova O.E., Mukhametshina N.E., Ageeva M.V., Mulyukin A.L., Gogolev Y.V. Formation of " nonculturable" dormant forms of the phytopathogenic enterobacterium Erwinia carotovora. Microbiology 2009, 78:585-592.
19. Gould W.D., Hagedorn C., Bardinelli T.R., Zablotowicz R.M. New selective media for enumeration and recovery of fluorescent pseudomonads from various habitats. Applied and Environmental Microbiology 1985, 49:28-32.
20. Grey B.E., Steck T.R. The viable but nonculturable state of Ralstonia solanacearum may be involved in long-term survival and plant infection. Applied and Environmental Microbiology 2001, 67:3866-3872.
21. Hagedorn C., Hansen D.T., Simonson G.H. Survival and movement of fecal indicator bacteria in soil under conditions of saturated flow. Journal of Environmental Quality 1978, 7:55-59.
22. Hase C., Mascher F., Moënne-Loccoz Y., Défago G. Nutrient deprivation and the subsequent survival of biocontrol Pseudomonas fluorescens CHA0 in soil. Soil Biology & Biochemistry 1999, 31:1181-1188.
23. Hase C., Hottinger M., Moënne-Loccoz Y., Défago G. Survival and cell culturability of biocontrol Pseudomonas fluorescens CHA0 in the rhizosphere of cucumber grown in two soils of contrasting fertility status. Biology and Fertility of Soils 2000, 32:217-221.
24. Heijnen C.E., Marinissen J.C.Y. Survival of bacteria introduced into soil by means of transport by Lumbricus rubellus. Biology and Fertility of Soils 1995, 20:63-69.
25. Heijnen C.E., Page S., van Elsas J.D. Metabolic activity of Flavobacterium strain P25 during starvation and after introduction into bulk soil and the rhizosphere of wheat. FEMS Microbiology Ecology 1995, 18:128-138.
26. Jäderlund L., Hellman M., Sundh I., Bailey M.J., Jansson J.K. Use of a novel nonantibiotic triple marker gene cassette to monitor high survival of Pseudomonas fluorescens SBW25 on winter wheat in the field. FEMS Microbiology Ecology 2008, 63:156-168.
27. Kana B.D., Mizrahi V. Resuscitation-promoting factors as lytic enzymes for bacterial growth and signaling. FEMS Immunology and Medical Microbiology 2010, 58:39-50.
28. Keel C., Défago G. Interactions between beneficial soil bacteria and root pathogens: mechanisms and ecological impact. Multitrophic Interactions in Terrestrial Ecosystems 1997, 27-46. Blackwell Science, London. A. Grange, V.K. Brown (Eds.).
29. Keel C., Weller D.M., Natsch A., Défago G., Cook R.J., Thomashow, L.S. Conservation of the 2,4-diacetylphloroglucinol biosynthesis locus among fluorescent Pseudomonas strains from diverse geographic locations. Applied and Environmental Microbiology 1996, 62:552-563.
30. Keer J.T., Birch L. Molecular methods for the assessment of bacterial viability. Journal of Microbiological Methods 2003, 53:175-183.
31. King E.O., Ward M.K., Raney D.E. Two simple media for the demonstration of pyocyanin and fluorescein. Journal of Laboratory and Clinical Medicine 1954, 44:301-307.
32. Kogure K., Simidu U., Taga N. A tentative direct microscopic method for counting living marine bacteria. Canadian Journal of Microbiology 1979, 25:415-420.
33. Kragelund L., Nybroe O. Culturability and expression of outer membrane proteins during carbon, nitrogen or phosphorus starvation of Pseudomonas fluorescens DF57 and P. putida DF14. Applied and Environmental Microbiology 1994, 60:2944-2948.
34. Langenbach T., Maciel S.J., Neves B.C.V., Hagler A.N., Mano D.M., Vugman N.V. Pseudomonas fluorescens dynamics in the soil surface to subsurface transect. Journal of Environmental Science and Health Part B 2006, 41:415-425.
35. Mascher F., Hase C., Moënne-Loccoz Y., Défago G. The viable but non-culturable state induced by abiotic stress in the biocontrol agent Pseudomonas fluorescens CHA0 does not promote strain persistence in soil. Applied and Environmental Microbiology 2000, 66:1662-1667.
36. Mascher F., Moënne-Loccoz Y., Schnider-Keel U., Keel C., Haas D., Défago G. Inactivation of the regulatory gene algU or gacA can affect the ability of biocontrol Pseudomonas fluorescens CHA0 to persist as culturable cells in nonsterile soil. Applied and Environmental Microbiology 2002, 68:2085-2088.
37. Mascher F., Schnider-Keel U., Haas D., Défago G., Moënne-Loccoz Y. Persistence and cell culturability of biocontrol Pseudomonas fluorescens CHA0 under plough pan conditions in soil and influence of the anaerobic regulator gene anr. Environmental Microbiology 2003, 5:103-115.
38. Natsch A., Keel C., Pfirter H.A., Haas D., Défago G. Contribution of the global regulator gene gacA to persistence and dissemination of Pseudomonas fluorescens biocontrol strain CHA0 introduced into soil microcosms. Applied and Environmental Microbiology 1994, 60:2553-2560.
39. Natsch A., Keel C., Troxler J., Zala M., von Albertini N., Défago G. Importance of preferential flow and soil management in vertical transport of a biocontrol strain of Pseudomonas fluorescens in structured field soil. Applied and Environmental Microbiology 1996, 62:33-40.
40. Nechitaylo T.Y., Yakimov M.M., Godinho M., Timmis K.N., Belogolova E., Byzov B.A., Kurakov A.V., Jones D.L., Golyshin P.N. Effect of the earthworms Lumbricus terrestris and Aporrectodea caliginosa on bacterial diversity in soil. Microbial Ecology 2010, 59:574-587.
41. Oliver J.D. Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiology Reviews 2010, 34:415-425.
42. Parle J.N. Microorganisms in the intestines of earthworms. Journal of General Microbiology 1963, 31:13-22.
43. Péchy-Tarr M., Bruck D.J., Maurhofer M., Fischer E., Vogne C., Henkels M.D., Donahue K.M., Grunder J., Loper J.E., Keel C. Molecular analysis of a novel gene cluster encoding an insect toxin in plant-associated strains of Pseudomonas fluorescens. Environmental Microbiology 2008, 10:2368-2386.
44. Pedersen J.C., Leser T.D. Survival of Enterobacter cloacae on leaves and in soil detected by immunofluorescence microscopy in comparison with selective plating. Microbial Releases 1992, 1:95-102.
45. Postma J., van Elsas J.D., Govaert J.M., van Veen J.A. The dynamics of Rhizobium leguminosarum biovar trifolii introduced soil as determined by immunofluorescence and selective technique. FEMS Microbiology Ecology 1988, 53:251-260.
46. Ramette A., Frapolli M., Fischer-Le Saux M., Gruffaz C., Meyer J.M., Défago G., Sutra L., Moënne-Loccoz Y. Pseudomonas protegens sp. nov., widespread plant-protecting bacteria producing the biocontrol compounds 2,4-diacetylphloroglucinol and pyoluteorin. Systematic and Applied Microbiology 2011, 34:180-188.
47. Recorbet G., Richaume A., Jocteur-Monrozier L. Distribution of a genetically-engineered Escherichia coli population introduced into soil. Letters in Applied Microbiology 1995, 21:38-40.
48. Reynolds P.J., Sharma P., Jenneman G.E., McInerney M.J. Mechanisms of microbial movement in subsurface materials. Applied and Environmental Microbiology 1989, 55:2280-2286.
49. Rezzonico F., Moënne-Loccoz Y., Défago G. Effect of stress on the ability of a phlA-based quantitative competitive PCR assay to monitor biocontrol strain Pseudomonas fluorescens CHA0. Applied and Environmental Microbiology 2003, 69:686-690.
50. Richter D.D., Markewitz D. How deep is soil?. Bioscience 1995, 45:600-609.
51. Ryder M.H., Pankhurst C.E., Rovira A.D., Correll R.L., Ophel Keller K.M. Detection of introduced bacteria in the rhizosphere using marker genes and DNA probes. Molecular Ecology of Rhizosphere Microorganisms 1994, 29-47. VCH Publishers, Weinheim. F. O'Gara, D. Dowling, B. Boesten (Eds.).
52. Smits T.H.M., Balada S.B., Witholt B., van Beilen J.B. Functional analysis of alkane hydroxylases from Gram-negative and Gram-positive bacteria. Journal of Bacteriology 2002, 184:1733-1742.
53. Stutz E.W., Défago G., Kern H. Naturally occurring fluorescent pseudomonads involved in suppression of black root rot of tobacco. Phytopathology 1986, 76:181-185.
54. Tan Y., Bond W.J., Rovira A.D., Brisbane P.G., Griffin D.M. Movement through soil of a biological control agent, Pseudomonas fluorescens. Soil Biology & Biochemistry 1992, 9:821-825.
55. Thompson I.P., Young C.S., Cook K.A., Letherbridge G., Burns R.G. Survival of two ecologically distinct bacteria (Flavobacterium and Arthrobacter) in unplanted and rhizosphere soil: field studies. Soil Biology & Biochemistry 1992, 24:1-14.
56. Troxler J., Berling C.H., Moënne-Loccoz Y., Keel C., Défago G. Interactions between the biocontrol agent Pseudomonas fluorescens CHA0 and Thielaviopsis basicola in tobacco roots observed by immunofluorescence microscopy. Plant Pathology 1997, 46:62-71.
57. Troxler J., Zala M., Moënne-Loccoz Y., Keel C., Défago G. Predominance of non-culturable cells of the biocontrol strain Pseudomonas fluorescens CHA0 in the surface horizon of large outdoor lysimeters. Applied and Environmental Microbiology 1997, 63:3776-3782.
58. van Elsas J.D., van Overbeek L.S. Bacterial responses to soil stimuli. Starvation in Bacteria 1993, 55-79. Plenum Press, New York. S. Kjelleberg (Ed.).
59. von Felten A., Défago G., Maurhofer M. Quantification of Pseudomonas fluorescens strains F113, CHA0 and Pf153 in the rhizosphere of maize by strain-specific real-time PCR unaffected by the variability of DNA extraction efficiency. Journal of Microbiological Methods 2010, 81:108-115.
60. Weller D.M., Thomashow L.S. Current challenges in introducing beneficial microorganisms into the rhizosphere. Molecular Ecology of Rhizosphere Microorganisms 1994, 1-18. VCH Publishers, Weinheim. F. O'Gara, D. Dowling, B. Boesten (Eds.).
61. Williams S.T. Oligotrophy in soil: fact or fiction?. Bacteria in Their Natural Environments 1985, 81-110. Academic Press, London. M. Fletcher, G.D. Floodgate (Eds.).