Home LiteratureArticle Details
PMID: 17601817 Published · ppublish English Journal Article

The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation.

Applied and environmental microbiology ·Vol. 73 ·No. 16 ·2007-08-00 ·Pages 5308-19

Caballero-Mellado J, Onofre-Lemus J, Estrada-de Los Santos P, Martínez-Aguilar L

Abstract

Burkholderia strains are promising candidates for biotechnological applications. Unfortunately, most of these strains belong to species of the Burkholderia cepacia complex (Bcc) involved in human infections, hampering potential applications. Novel diazotrophic Burkholderia species, phylogenetically distant from the Bcc species, have been discovered recently, but their environmental distribution and relevant features for agro-biotechnological applications are little known. In this work, the occurrence of N2-fixing Burkholderia species in the rhizospheres and rhizoplanes of tomato plants field grown in Mexico was assessed. The results revealed a high level of diversity of diazotrophic Burkholderia species, including B. unamae, B. xenovorans, B. tropica, and two other unknown species, one of them phylogenetically closely related to B. kururiensis. These N2-fixing Burkholderia species exhibited activities involved in bioremediation, plant growth promotion, or biological control in vitro. Remarkably, B. unamae and B. kururiensis grew with aromatic compounds (phenol and benzene) as carbon sources, and the presence of aromatic oxygenase genes was confirmed in both species. The rhizospheric and endophyte nature of B. unamae and its ability to degrade aromatic compounds suggest that it could be used in rhizoremediation and for improvement of phytoremediation. B. kururiensis and other Burkholderia sp. strains grew with toluene. B. unamae and B. xenovorans exhibited ACC (1-aminocyclopropane-1-carboxylic acid) deaminase activity, and the occurrence of acdS genes encoding ACC deaminase was confirmed. Mineral phosphate solubilization through organic acid production appears to be the mechanism used by most diazotrophic Burkholderia species, but in B. tropica, there presumably exists an additional unknown mechanism. Most of the diazotrophic Burkholderia species produced hydroxamate-type siderophores. Certainly, the N2-fixing Burkholderia species associated with plants have great potential for agro-biotechnological applications.

MeSH Terms
Agriculture/methods Biodegradation, Environmental Burkholderia/classification,genetics,metabolism Electrophoresis, Polyacrylamide Gel Lycopersicon esculentum/microbiology Molecular Sequence Data Nitrogen Fixation Phosphates/metabolism Phylogeny Plant Roots/microbiology Polymerase Chain Reaction RNA, Ribosomal, 16S/genetics Sequence Analysis, DNA Siderophores/metabolism Soil Microbiology
Chemicals
Phosphates RNA, Ribosomal, 16S Siderophores
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Caballero-Mellado Jesús
Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Ap. Postal 565-A, Cuernavaca, Morelos, México. jesuscab@ccg.unam.mx
Onofre-Lemus Janette
Estrada-de Los Santos Paulina
Martínez-Aguilar Lourdes
References (63)
63 references, click to expand
  1. Molecular method to assess the diversity of Burkholderia species in environmental samples.
    Appl Environ Microbiol. 2002 Apr;68(4):1595-603 PMID: 11916673
  2. Multivariate analyses of Burkholderia species in soil: effect of crop and land use history.
    Appl Environ Microbiol. 2004 Jul;70(7):4012-20 PMID: 15240277
  3. Isolation and characterization of ACC deaminase genes from two different plant growth-promoting rhizobacteria.
    Can J Microbiol. 1998 Sep;44(9):833-43 PMID: 9851025
  4. Endophytic nitrogen fixation in dune grasses (Ammophila arenaria and Elymus mollis) from Oregon.
    FEMS Microbiol Ecol. 2004 Sep 1;49(3):469-79 PMID: 19712295
  5. Classification of the biphenyl- and polychlorinated biphenyl-degrading strain LB400T and relatives as Burkholderia xenovorans sp. nov.
    Int J Syst Evol Microbiol. 2004 Sep;54(Pt 5):1677-81 PMID: 15388727
  6. Burkholderia terrae sp. nov., isolated from a forest soil.
    Int J Syst Evol Microbiol. 2006 Feb;56(Pt 2):453-7 PMID: 16449457
  7. The neighbor-joining method: a new method for reconstructing phylogenetic trees.
    Mol Biol Evol. 1987 Jul;4(4):406-25 PMID: 3447015
  8. Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography.
    FEMS Microbiol Ecol. 2006 Jun;56(3):455-70 PMID: 16689877
  9. Universal chemical assay for the detection and determination of siderophores.
    Anal Biochem. 1987 Jan;160(1):47-56 PMID: 2952030
  10. Polyhydroxyalkanoate-accumulating bacterium isolated from soil of a sugar-cane plantation in Brazil.
    Int J Syst Evol Microbiol. 2001 Sep;51(Pt 5):1709-13 PMID: 11594600
  11. Proof that Burkholderia strains form effective symbioses with legumes: a study of novel Mimosa-nodulating strains from South America.
    Appl Environ Microbiol. 2005 Nov;71(11):7461-71 PMID: 16269788
  12. Systemic resistance induced by rhizosphere bacteria.
    Annu Rev Phytopathol. 1998;36:453-83 PMID: 15012509
  13. Nitrogen fixation--assay methods and techniques.
    Methods Enzymol. 1972;24:415-31 PMID: 4206744
  14. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects.
    Appl Environ Microbiol. 2005 Sep;71(9):4951-9 PMID: 16151072
  15. A N2-fixing endophytic Burkholderia sp. associated with maize plants cultivated in Mexico.
    Can J Microbiol. 2002 Apr;48(4):285-94 PMID: 12030700
  16. Gut symbiotic bacteria of the genus Burkholderia in the broad-headed bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae).
    Appl Environ Microbiol. 2005 Jul;71(7):4035-43 PMID: 16000818
  17. Nucleotide sequencing and transcriptional mapping of the genes encoding biphenyl dioxygenase, a multicomponent polychlorinated-biphenyl-degrading enzyme in Pseudomonas strain LB400.
    J Bacteriol. 1992 May;174(9):2903-12 PMID: 1569021
  18. Phosphate solubilizing bacteria and their role in plant growth promotion.
    Biotechnol Adv. 1999 Oct;17(4-5):319-39 PMID: 14538133
  19. Culture-based and non-growth-dependent detection of the Burkholderia cepacia complex in soil environments.
    Appl Environ Microbiol. 2002 Aug;68(8):3750-8 PMID: 12147469
  20. Burkholderia ferrariae sp. nov., isolated from an iron ore in Brazil.
    Int J Syst Evol Microbiol. 2006 Oct;56(Pt 10):2421-5 PMID: 17012573
  21. 16S ribosomal DNA amplification for phylogenetic study.
    J Bacteriol. 1991 Jan;173(2):697-703 PMID: 1987160
  22. Metabolic diversity in aromatic compound utilization by anaerobic microbes.
    Annu Rev Microbiol. 2002;56:345-69 PMID: 12142480
  23. Burkholderia mimosarum sp. nov., isolated from root nodules of Mimosa spp. from Taiwan and South America.
    Int J Syst Evol Microbiol. 2006 Aug;56(Pt 8):1847-51 PMID: 16902019
  24. Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains.
    Appl Environ Microbiol. 1999 Jun;65(6):2429-38 PMID: 10347023
  25. Stable isotope probing reveals the dominant role of Burkholderia species in aerobic degradation of PCBs.
    FEMS Microbiol Ecol. 2005 Apr 1;52(2):207-17 PMID: 16329907
  26. Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil.
    Appl Environ Microbiol. 2002 Aug;68(8):3818-29 PMID: 12147477
  27. Genetic analysis of a Pseudomonas locus encoding a pathway for biphenyl/polychlorinated biphenyl degradation.
    Gene. 1993 Aug 16;130(1):47-55 PMID: 8344527
  28. Biotechnological potential within the genus Burkholderia.
    Lett Appl Microbiol. 2005;41(1):8-11 PMID: 15960745
  29. Burkholderia tropica sp. nov., a novel nitrogen-fixing, plant-associated bacterium.
    Int J Syst Evol Microbiol. 2004 Nov;54(Pt 6):2155-62 PMID: 15545451
  30. Transformation of Azospirillum brasilense Cd with an ACC deaminase gene from enterobacter cloacae UW4 fused to the Tet r gene promoter improves its fitness and plant growth promoting ability.
    Microb Ecol. 2003 Jul;46(1):122-33 PMID: 12739073
  31. Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants.
    Nat Biotechnol. 2004 May;22(5):583-8 PMID: 15077119
  32. Mathematical model for studying genetic variation in terms of restriction endonucleases.
    Proc Natl Acad Sci U S A. 1979 Oct;76(10):5269-73 PMID: 291943
  33. Discrimination of Burkholderia multivorans and Burkholderia vietnamiensis from Burkholderia cepacia genomovars I, III, and IV by PCR.
    J Clin Microbiol. 1999 May;37(5):1335-9 PMID: 10203482
  34. [Bacteria of the genus Burkholderia as a typical component of the microbial community of sphagnum peat bogs].
    Mikrobiologiia. 2006 Jan-Feb;75(1):110-7 PMID: 16579452
  35. The species concept for prokaryotes.
    FEMS Microbiol Rev. 2001 Jan;25(1):39-67 PMID: 11152940
  36. Horizontal gene transfer to endogenous endophytic bacteria from poplar improves phytoremediation of toluene.
    Appl Environ Microbiol. 2005 Dec;71(12):8500-5 PMID: 16332840
  37. Species abundance and diversity of Burkholderia cepacia complex in the environment.
    Appl Environ Microbiol. 2005 Mar;71(3):1193-201 PMID: 15746318
  38. Detection and enumeration of aromatic oxygenase genes by multiplex and real-time PCR.
    Appl Environ Microbiol. 2003 Jun;69(6):3350-8 PMID: 12788736
  39. Selected phenolic compounds in cultivated plants: ecologic functions, health implications, and modulation by pesticides.
    Environ Health Perspect. 1999 Feb;107 Suppl 1:109-14 PMID: 10229712
  40. Burkholderia phenoliruptrix sp. nov., to accommodate the 2,4,5-trichlorophenoxyacetic acid and halophenol-degrading strain AC1100.
    Syst Appl Microbiol. 2004 Nov;27(6):623-7 PMID: 15612618
  41. Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes.
    Syst Appl Microbiol. 2002 Dec;25(4):507-12 PMID: 12583710
  42. Burkholderia kururiensis sp. nov., a trichloroethylene (TCE)-degrading bacterium isolated from an aquifer polluted with TCE.
    Int J Syst Evol Microbiol. 2000 Mar;50 Pt 2:743-9 PMID: 10758884
  43. Non-Frankia actinomycetes isolated from surface-sterilized roots of Casuarina equisetifolia fix nitrogen.
    Appl Environ Microbiol. 2005 Jan;71(1):460-6 PMID: 15640222
  44. Characterization of amplified polymerase chain reaction glnB and nifH gene fragments of nitrogen-fixing Burkholderia species.
    Lett Appl Microbiol. 2003;36(2):77-82 PMID: 12535125
  45. MEGA2: molecular evolutionary genetics analysis software.
    Bioinformatics. 2001 Dec;17(12):1244-5 PMID: 11751241
  46. Diversity and significance of Burkholderia species occupying diverse ecological niches.
    Environ Microbiol. 2003 Sep;5(9):719-29 PMID: 12919407
  47. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms.
    FEMS Microbiol Lett. 1999 Jan 1;170(1):265-70 PMID: 9919677
  48. Diazotrophic burkholderia species associated with field-grown maize and sugarcane.
    Appl Environ Microbiol. 2006 May;72(5):3103-10 PMID: 16672447
  49. Use of siderophores to type pseudomonads: the three Pseudomonas aeruginosa pyoverdine systems.
    Microbiology. 1997 Jan;143 ( Pt 1):35-43 PMID: 9025276
  50. Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution.
    Appl Environ Microbiol. 2001 Jun;67(6):2790-8 PMID: 11375196
  51. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  52. The multifarious, multireplicon Burkholderia cepacia complex.
    Nat Rev Microbiol. 2005 Feb;3(2):144-56 PMID: 15643431
  53. A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria
    J Theor Biol. 1998 Jan 7;190(1):63-8 PMID: 9473391
  54. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  55. Polyphasic taxonomy, a consensus approach to bacterial systematics.
    Microbiol Rev. 1996 Jun;60(2):407-38 PMID: 8801440
  56. Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility.
    Proc Natl Acad Sci U S A. 2006 Oct 17;103(42):15280-7 PMID: 17030797
  57. Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil.
    Res Microbiol. 2001 Jan-Feb;152(1):95-103 PMID: 11281330
  58. Involvement of two plasmids in fenitrothion degradation by Burkholderia sp. strain NF100.
    Appl Environ Microbiol. 2000 Apr;66(4):1737-40 PMID: 10742273
  59. Burkholderia unamae sp. nov., an N2-fixing rhizospheric and endophytic species.
    Int J Syst Evol Microbiol. 2004 Jul;54(Pt 4):1165-72 PMID: 15280286
  60. Assessment of toluene/biphenyl dioxygenase gene diversity in benzene-polluted soils: links between benzene biodegradation and genes similar to those encoding isopropylbenzene dioxygenases.
    Appl Environ Microbiol. 2006 May;72(5):3504-14 PMID: 16672497
  61. Burkholderia cepacia complex species: health hazards and biotechnological potential.
    Trends Microbiol. 2006 Jun;14(6):277-86 PMID: 16684604
  62. Burkholderia silvatlantica sp. nov., a diazotrophic bacterium associated with sugar cane and maize.
    Int J Syst Evol Microbiol. 2006 Aug;56(Pt 8):1931-7 PMID: 16902033
  63. Absence of siderophore activity in Legionella species grown in iron-deficient media.
    J Bacteriol. 1983 Apr;154(1):324-9 PMID: 6219988
Article Info
Journal
Applied and environmental microbiology
Abbr.
Appl Environ Microbiol
ISSN
0099-2240
Published
2007-08-00
Epub
2007-00-29
Pages
5308-19
Language
English
Region
United States
NLM ID
7605801
PMCID
PMC1950987
Subset
IM
Databases
GENBANK
EF139178, EF139179, EF139180, EF139181, EF139182, EF139183, EF139184, EF139185, EF139186, EF139187, EF139188, EF151008, EF151009, EF151010, EF151011, EF151012, EF151013, EF158449, EF408192, EF408193, EF408194
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com