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PMID: 16751545 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Potential of a 16S rRNA-based taxonomic microarray for analyzing the rhizosphere effects of maize on Agrobacterium spp. and bacterial communities.

Applied and environmental microbiology ·Vol. 72 ·No. 6 ·2006-06-00 ·Pages 4302-12

Sanguin H, Remenant B, Dechesne A, Thioulouse J, Vogel TM, Nesme X, Moënne-Loccoz Y, Grundmann GL

Abstract

Bacterial diversity is central to ecosystem sustainability and soil biological function, for which the role of roots is important. The high-throughput analysis potential of taxonomic microarray should match the breadth of bacterial diversity. Here, the power of this technology was evidenced through methodological verifications and analysis of maize rhizosphere effect based on a 16S rRNA-based microarray developed from the prototype of H. Sanguin et al. (Environ. Microbiol. 8:289-307, 2006). The current probe set was composed of 170 probes (41 new probes in this work) that targeted essentially the Proteobacteria. Cloning and sequencing of 16S rRNA amplicons were carried out on maize rhizosphere and bulk soil DNA. All tested clones that had a perfect match with corresponding probes were positive in the hybridization experiment. The hierarchically nested probes were reliable, but the level of taxonomic identification was variable, depending on the probe set specificity. The comparison of experimental and theoretical hybridizations revealed 0.91% false positives and 0.81% false negatives. The microarray detection threshold was estimated at 0.03% of a given DNA type based on DNA spiking experiments. A comparison of the maize rhizosphere and bulk soil hybridization results showed a significant rhizosphere effect, with a higher predominance of Agrobacterium spp. in the rhizosphere, as well as a lower prevalence of Acidobacteria, Bacteroidetes, Verrucomicrobia, and Planctomycetes, a new taxon of interest in soil. In addition, well-known taxonomic groups such as Sphingomonas spp., Rhizobiaceae, and Actinobacteria were identified in both microbial habitats with strong hybridization signals. The taxonomic microarray developed in the present study was able to discriminate and characterize bacterial community composition in related biological samples, offering extensive possibilities for systematic exploration of bacterial diversity in ecosystems.

MeSH Terms
Cloning, Molecular Oligonucleotide Array Sequence Analysis Phylogeny Polymerase Chain Reaction Proteobacteria/classification,genetics,growth & development RNA, Bacterial/genetics RNA, Ribosomal, 16S/genetics Rhizobium/classification,genetics,growth & development Soil Microbiology Zea mays/microbiology
Chemicals
RNA, Bacterial RNA, Ribosomal, 16S
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Sanguin Hervé
UMR CNRS 5557/USC INRA 1193 Ecologie Microbienne, Université Claude Bernard (Lyon 1), 43 bd du 11 Novembre 1918, F-69622 Villeurbanne Cedex, France.
Remenant Benoît
Dechesne Arnaud
Thioulouse Jean
Vogel Timothy M
Nesme Xavier
Moënne-Loccoz Yvan
Grundmann Geneviève L
References (75)
75 references, click to expand
  1. The planctomycetes: emerging models for microbial ecology, evolution and cell biology.
    Microbiology. 1995 Jul;141 ( Pt 7):1493-506 PMID: 7551018
  2. Relationship between spatial and genetic distance in Agrobacterium spp. in 1 cubic centimeter of soil.
    Appl Environ Microbiol. 2003 Mar;69(3):1482-7 PMID: 12620832
  3. Development of a universal microarray based on the ligation detection reaction and 16S rrna gene polymorphism to target diversity of cyanobacteria.
    Appl Environ Microbiol. 2004 Dec;70(12):7161-72 PMID: 15574913
  4. Monitoring a widespread bacterial group: in situ detection of planctomycetes with 16S rRNA-targeted probes.
    Microbiology. 1998 Dec;144 ( Pt 12):3257-66 PMID: 9884217
  5. Studies on the microbial populations of the rhizosphere of big sagebrush ( Artemisia tridentata).
    J Ind Microbiol Biotechnol. 2004 Jul;31(6):278-88 PMID: 15221668
  6. probeBase: an online resource for rRNA-targeted oligonucleotide probes.
    Nucleic Acids Res. 2003 Jan 1;31(1):514-6 PMID: 12520066
  7. The limits of log-ratios.
    BMC Biotechnol. 2004 Mar 8;4:3 PMID: 15113428
  8. Development and evaluation of functional gene arrays for detection of selected genes in the environment.
    Appl Environ Microbiol. 2001 Dec;67(12):5780-90 PMID: 11722935
  9. Prokaryotic diversity and its limits: microbial community structure in nature and implications for microbial ecology.
    Curr Opin Microbiol. 2004 Jun;7(3):221-6 PMID: 15196488
  10. Bacterial Community Structure in Relation to the Carbon Environments in Lettuce and Tomato Rhizospheres and in Bulk Soil
    Microb Ecol. 1997 Sep;34(2):109-17 PMID: 9230098
  11. Microbial co-operation in the rhizosphere.
    J Exp Bot. 2005 Jul;56(417):1761-78 PMID: 15911555
  12. Importance of replication in microarray gene expression studies: statistical methods and evidence from repetitive cDNA hybridizations.
    Proc Natl Acad Sci U S A. 2000 Aug 29;97(18):9834-9 PMID: 10963655
  13. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity.
    J Bacteriol. 1998 Sep;180(18):4765-74 PMID: 9733676
  14. Molecular evidence for novel planctomycete diversity in a municipal wastewater treatment plant.
    Appl Environ Microbiol. 2003 Dec;69(12):7354-63 PMID: 14660385
  15. Molecular profiling of rhizosphere microbial communities associated with healthy and diseased black spruce (Picea mariana) seedlings grown in a nursery.
    Appl Environ Microbiol. 2004 Jun;70(6):3541-51 PMID: 15184155
  16. Radioisotopic, culture-based, and oligonucleotide microchip analyses of thermophilic microbial communities in a continental high-temperature petroleum reservoir.
    Appl Environ Microbiol. 2003 Oct;69(10):6143-51 PMID: 14532074
  17. Design and application of an oligonucleotide microarray for the investigation of compost microbial communities.
    J Microbiol Methods. 2005 Jul;62(1):37-56 PMID: 15823393
  18. Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods.
    Appl Environ Microbiol. 2001 May;67(5):2284-91 PMID: 11319113
  19. Prokaryotes: the unseen majority.
    Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):6578-83 PMID: 9618454
  20. Rapid quantification and taxonomic classification of environmental DNA from both prokaryotic and eukaryotic origins using a microarray.
    FEMS Microbiol Lett. 2005 Apr 15;245(2):271-8 PMID: 15837382
  21. A census of rRNA genes and linked genomic sequences within a soil metagenomic library.
    Appl Environ Microbiol. 2003 May;69(5):2684-91 PMID: 12732537
  22. Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia.
    Appl Environ Microbiol. 2002 May;68(5):2391-6 PMID: 11976113
  23. In situ visualization of high genetic diversity in a natural microbial community.
    J Bacteriol. 1996 Jun;178(12):3496-500 PMID: 8655546
  24. Amplification of DNA from native populations of soil bacteria by using the polymerase chain reaction.
    Appl Environ Microbiol. 1992 Oct;58(10):3413-6 PMID: 1444376
  25. Diversity and seasonal changes of uncultured Planctomycetales in river biofilms.
    Appl Environ Microbiol. 2004 Sep;70(9):5094-101 PMID: 15345387
  26. Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed.
    Appl Environ Microbiol. 2001 Oct;67(10):4742-51 PMID: 11571180
  27. Unravelling rhizosphere-microbial interactions: opportunities and limitations.
    Trends Microbiol. 2004 Aug;12(8):386-93 PMID: 15276615
  28. Application of rRNA-targeted oligonucleotide probes in biotechnology.
    Appl Microbiol Biotechnol. 2001 Jul;56(1-2):40-57 PMID: 11499947
  29. The isotope array, a new tool that employs substrate-mediated labeling of rRNA for determination of microbial community structure and function.
    Appl Environ Microbiol. 2003 Nov;69(11):6875-87 PMID: 14602652
  30. Microbial populations responsible for specific soil suppressiveness to plant pathogens.
    Annu Rev Phytopathol. 2002;40:309-48 PMID: 12147763
  31. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias.
    Bioinformatics. 2003 Jan 22;19(2):185-93 PMID: 12538238
  32. Stability and variability in competitive communities.
    Science. 1999 Oct 15;286(5439):542-4 PMID: 10521351
  33. Levels of bacterial community diversity in four arid soils compared by cultivation and 16S rRNA gene cloning.
    Appl Environ Microbiol. 1999 Apr;65(4):1662-9 PMID: 10103265
  34. High-density microarray of small-subunit ribosomal DNA probes.
    Appl Environ Microbiol. 2002 May;68(5):2535-41 PMID: 11976131
  35. Fingerprinting diazotroph communities in the Chesapeake Bay by using a DNA macroarray.
    Appl Environ Microbiol. 2004 Mar;70(3):1767-76 PMID: 15006803
  36. Quantitative detection of microbial genes by using DNA microarrays.
    Appl Environ Microbiol. 2002 Mar;68(3):1425-30 PMID: 11872496
  37. Evaluation of 50-mer oligonucleotide arrays for detecting microbial populations in environmental samples.
    Biotechniques. 2004 Apr;36(4):664-70, 672, 674-5 PMID: 15088384
  38. Temporal Changes in the Bacterial Communities of Soil, Rhizosphere, and Endorhiza Associated with Field-Grown Cucumber (Cucumis sativus L.)
    Microb Ecol. 1997 Nov;34(3):210-23 PMID: 9337416
  39. A variance-stabilizing transformation for gene-expression microarray data.
    Bioinformatics. 2002;18 Suppl 1:S105-10 PMID: 12169537
  40. 16S rRNA gene-based oligonucleotide microarray for environmental monitoring of the betaproteobacterial order "Rhodocyclales".
    Appl Environ Microbiol. 2005 Mar;71(3):1373-86 PMID: 15746340
  41. Microarray and functional gene analyses of sulfate-reducing prokaryotes in low-sulfate, acidic fens reveal cooccurrence of recognized genera and novel lineages.
    Appl Environ Microbiol. 2004 Dec;70(12):6998-7009 PMID: 15574893
  42. The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set.
    Syst Appl Microbiol. 1999 Sep;22(3):434-44 PMID: 10553296
  43. A new approach for the analysis of bacterial microarray-based Comparative Genomic Hybridization: insights from an empirical study.
    BMC Genomics. 2005;6:78 PMID: 15918914
  44. The Diversity of Archaea and Bacteria in Association with the Roots of Zea mays L.
    Microb Ecol. 2001 Apr;41(3):252-263 PMID: 11391463
  45. Phytoremediation.
    Annu Rev Plant Biol. 2005;56:15-39 PMID: 15862088
  46. Detection and in situ identification of representatives of a widely distributed new bacterial phylum.
    FEMS Microbiol Lett. 1997 Aug 1;153(1):181-90 PMID: 9252585
  47. The effects of copper on the microbial community of a coral reef sponge.
    Environ Microbiol. 2001 Jan;3(1):19-31 PMID: 11225720
  48. Identification of planctomycetes with order-, genus-, and strain-specific 16S rRNA-targeted probes.
    Microb Ecol. 2004 Apr;47(3):243-51 PMID: 14994173
  49. Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA.
    Appl Environ Microbiol. 1997 Nov;63(11):4516-22 PMID: 9361437
  50. Effects of growth medium, inoculum size, and incubation time on culturability and isolation of soil bacteria.
    Appl Environ Microbiol. 2005 Feb;71(2):826-34 PMID: 15691937
  51. Denitrifying bacteria in bulk and maize-rhizospheric soil: diversity and N2O-reducing abilities.
    Can J Microbiol. 2004 Jul;50(7):469-74 PMID: 15381970
  52. Environmental factors influencing the distribution of rRNA from Verrucomicrobia in soil.
    FEMS Microbiol Ecol. 2001 Mar;35(1):105-112 PMID: 11248395
  53. Direct detection of 16S rRNA in soil extracts by using oligonucleotide microarrays.
    Appl Environ Microbiol. 2001 Oct;67(10):4708-16 PMID: 11571176
  54. Molecular analysis of the nitrate-reducing community from unplanted and maize-planted soils.
    Appl Environ Microbiol. 2002 Dec;68(12):6121-8 PMID: 12450836
  55. Improving the scaling normalization for high-density oligonucleotide GeneChip expression microarrays.
    BMC Bioinformatics. 2004 Jul 29;5:103 PMID: 15283861
  56. ARB: a software environment for sequence data.
    Nucleic Acids Res. 2004;32(4):1363-71 PMID: 14985472
  57. Environmental application of array technology: promise, problems and practicalities.
    Curr Opin Biotechnol. 2003 Jun;14(3):311-8 PMID: 12849785
  58. Optimization of diagnostic microarray for application in analysing landfill methanotroph communities under different plant covers.
    Environ Microbiol. 2004 Apr;6(4):347-63 PMID: 15008813
  59. Prevalence of fluorescent pseudomonads producing antifungal phloroglucinols and/or hydrogen cyanide in soils naturally suppressive or conducive to tobacco black root rot.
    FEMS Microbiol Ecol. 2003 May 1;44(1):35-43 PMID: 19719649
  60. Bacterial diversity in maize rhizospheres: conclusions on the use of genetic profiles based on PCR-amplified partial small subunit rRNA genes in ecological studies.
    Mol Ecol. 2003 Jan;12(1):251-62 PMID: 12492893
  61. Comparative 16S rDNA and 16S rRNA sequence analysis indicates that Actinobacteria might be a dominant part of the metabolically active bacteria in heavy metal-contaminated bulk and rhizosphere soil.
    Environ Microbiol. 2003 Oct;5(10):896-907 PMID: 14510843
  62. Effect of carbon and nitrogen input on the bacterial community structure of Neocaledonian nickel mine spoils.
    FEMS Microbiol Ecol. 2005 Feb 1;51(3):333-40 PMID: 16329881
  63. Bellerophon: a program to detect chimeric sequences in multiple sequence alignments.
    Bioinformatics. 2004 Sep 22;20(14):2317-9 PMID: 15073015
  64. Development and validation of a diagnostic microbial microarray for methanotrophs.
    Environ Microbiol. 2003 Jul;5(7):566-82 PMID: 12823189
  65. Characterization of the unlinked 16S rDNA and 23S-5S rRNA operon of Wolbachia pipientis, a prokaryotic parasite of insect gonads.
    Gene. 1995 Nov 7;165(1):81-6 PMID: 7489921
  66. Development and validation of a prototype 16S rRNA-based taxonomic microarray for Alphaproteobacteria.
    Environ Microbiol. 2006 Feb;8(2):289-307 PMID: 16423016
  67. Efficient procedure for purification of obligate intracellular Wolbachia pipientis and representative amplification of its genome by multiple-displacement amplification.
    Appl Environ Microbiol. 2005 Nov;71(11):6910-7 PMID: 16269725
  68. Diversity and dynamics of microbial communities in soils from agro-ecosystems.
    Environ Microbiol. 2003 Jun;5(6):441-52 PMID: 12755711
  69. Terminal restriction pattern analysis of 16S rRNA genes for the characterization of bacterial communities of activated sludge.
    J Biosci Bioeng. 2000;90(2):148-56 PMID: 16232834
  70. Parallel characterization of anaerobic toluene- and ethylbenzene-degrading microbial consortia by PCR-denaturing gradient gel electrophoresis, RNA-DNA membrane hybridization, and DNA microarray technology.
    Appl Environ Microbiol. 2002 Jul;68(7):3215-25 PMID: 12088997
  71. Validation of a more sensitive method for using spotted oligonucleotide DNA microarrays for functional genomics studies on bacterial communities.
    Environ Microbiol. 2003 Oct;5(10):933-43 PMID: 14510847
  72. Application and validation of DNA microarrays for the 16S rRNA-based analysis of marine bacterioplankton.
    Environ Microbiol. 2004 Jun;6(6):638-45 PMID: 15142252
  73. Unraveling the extent of diversity within the order Planctomycetales.
    Appl Environ Microbiol. 1995 Jun;61(6):2270-5 PMID: 7793948
  74. The diversity-stability debate.
    Nature. 2000 May 11;405(6783):228-33 PMID: 10821283
  75. Exploration, normalization, and summaries of high density oligonucleotide array probe level data.
    Biostatistics. 2003 Apr;4(2):249-64 PMID: 12925520
Article Info
Journal
Applied and environmental microbiology
Abbr.
Appl Environ Microbiol
ISSN
0099-2240
Published
2006-06-00
Pages
4302-12
Language
English
Region
United States
NLM ID
7605801
PMCID
PMC1489601
Subset
IM
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