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Microorganisms play an essential role in maintaining soil fertility: cycling nutrients, influencing their availability; improving soil structure; supporting healthy plant growth; degrading organic pollutants. Some soil bacteria and fungi cause plant diseases; others are antagonistic to plant pathogens and invertebrate pests. The rhizosphere provides a region of increased microbial activity in which certain groups of bacteria and fungi are more likely to proliferate than in the bulk soil.
Soil and rhizosphere microbial ecology
Some rhizosphere microorganisms originate from the seed but the majority are derived from the soil in which a plant is growing, and they will be returned to the soil, thus bulk soil and rhizosphere reciprocate impact on microbial communities. This is especially important in the case of plant pathogenic microorganisms and microbial antagonists to pests and pathogens. Any one group of microbes is unlikely to perform with maximum efficiency under all circumstances so genetically diverse populations are needed to provide continuation of important soil processes. Since the relationship between the size, diversity and activity of microbial populations and soil 'quality' is unclear, also how these properties fluctuate throughout the seasons, with crop rotations, and the scale (temporal, spatial) on which they vary, it is difficult to predict effects of changes in agricultural practice, land use, climate, introduction of novel plants, microbial inoculants and pollution on soil quality. |
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Baseline studies are needed to demonstrate the significance of any observed changes in response to unusual stress. Some functions undertaken by specific groups of bacteria can be measured in situ and may indicate the size of the active population, but cannot describe its diversity or indicate if there is a related, inactive population. Advances in molecular techniques mean that more detailed examination of individual groups and of the total microbial population is possible, whether or not they can be isolated from the soil and be grown in laboratory culture. Because the genetic material defines organism identity, profiles based on DNA are the most reliable method of identification, including difficult-to-culture microbes. The available DNA sequence information on environmental bacteria is increasing exponentially, enabling design of many group- and species-specific primers. PCR techniques can be used to amplify sequences from individual or related strains in nucleic acids (DNA or RNA) isolated from soil providing estimates of activity, diversity and relative abundance. Quantitative PCR can estimate the frequency of sequences and reverse transcriptase PCR can amplify ribosomal sequences and functional genes identifying which populations are active. However, to assess and compare whole populations, DNA arrays offer great future possibilities.
Bacterial cell showing properties that can be measured directly from soil
The application of modern molecular techniques to study the ecology of soil fungi lags behind bacteria. Several groups of soil fungi are known to attack plant pathogenic nematodes, and have potential as biological control agents. To exploit fungal agents, or to manage the development of naturally suppressive soils, further understanding of fungal biology and ecology, especially genetic diversity and population dynamics, is important.
Monitoring
survival and impact of bacteria introduced into the field
Microbial
diversity in soils
Nitrification, the conversion of ammonia to nitrate
Genetic
diversity and culturability of bacteria of archived Broadbalk soil samples
Could
genetically modified plants adversely impact soil biology
Bacterial community structure in the rhizosphere
Denitrification, the reduction of nitrate to oxides of nitrogen
Metagenomics - a technique for cloning functional genes
The nematophagous
fungusPochonia chlamydosporia
Fungal interactions in the rhizosphere
Transformation of fungi with marker genes
1. Johnston, A.W.B., Beynon, J.L., Buchanan–Wollaston, A.V., Setchell, S.M. Hirsch, P.R. & Beringer, J.E. (1978) High frequency transfer of nodulating ability between strains and species of Rhizobium. Nature 276, 635–636.
2. Hirsch, P.R,. (1979) Plasmid determined bacteriocin production by Rhizobium leguminosarum. Journal of General Microbiology 113, 219–228.
3. Johnston, A.W.B., Beringer, J.E., Beynon, J.L., Brewin, N., Buchanan–Wollaston, A.V. & Hirsch, P.R,. (1979) Plasmids and the Rhizobium–legume symbiosis. In: Plasmids of Medical, Environmental and Commercial Importance. Eds. K.N. Timmis & A. Puhler, Elsevier Amsterdam.
4. Brewin, N.J., Beringer, J.E., Buchanan–Wollaston, A.V., Johnston, A.W.B. & Hirsch, P.R,. (1980) Transfer of symbiotic genes with bacteriocinogenic plasmids in Rhizobium leguminosarum. Journal of General Microbiology 116, 261–270.
5. Buchanan–Wollaston, A.V., Beringer, J.E., Brewin, N.J., Hirsch, P.R,. & Johnston, A.W.B. (1980) Isolation of symbiotically defective mutants in Rhizobium leguminosarum by insertion of the transposon Tn5 into a transmissible plasmid. Molecular and General Genetics 178, 185–190.
6. Hirsch, P.R,., Van Montagu, M., Johnston, A.W.B., Brewin, N.J. & Schell, J. (1980) Physical identification of bacteriocinogenic, nodulation and other plasmids in strains of Rhizobium leguminosarum. Journal of General Microbiology 120, 403–412.
7. Hoekema, A., Hirsch, P.R,., Hooykaas, P.J.J. & Schilperoort, R.A. (1983) A binary plant vector strategy based on separation of vir– and T–region of the Agrobacterium tumefaciens Ti–plasmid. Nature 303, 179–180.
8. Beringer, J.E. & Hirsch, P.R,. (1984) Genetic engineering and nitrogen fixation. Biotechnology and Genetic Engineering Reviews 1, 65–88.
9. Hirsch, P.R,. & Beggs, J.D. (1984) Agrobacterium tumefaciens T–DNA in the yeast Saccharomyces cerevisiae. Molecular and General Genetics 195, 209–214.
10. Beringer, J.E. & Hirsch, P.R,. (1984) The role of plasmids in microbial ecology. In: Current Perspectives in Microbial Ecology. Eds. M.J.Klug & C.M. Reddy, American Society for Microbiology, Washington.
11. Hirsch, P.R,. & Beringer, J.E. (1984) A physical map of pPH1JI and pJB4JI. Plasmid 12, 139–141.
12. Hirsch, P.R,. (1984) Improved crop plant productivity through genetic manipulation of mycorrhizal fungi? Chemistry and Industry 23, 833–838.
13. Wang, C.L., Spokes, J.R., Woodward, M.J. & Hirsch, P.R,. (1985) Transposon mutagenesis of Rhizobium using a derivative
of Tn5 conferring gentamicin and spectinomycin resistance. In: Nitrogen Fixation Research
Progress. Eds. Evans, H.J., Bottomley, P.J. & Newton, W.E. Nijhoff/Junk, The Hague, The
14. Hirsch, P.R,. (1986) Gene cloning and its potential application to mycorrhizal fungi.
Physiological and Genetical Aspects of Mycorrhizae. Proceedings of the 1st European Conference on Mycorrhizae, Dijon,
15. Wang, C.L., Beringer, J.E. & Hirsch, P.R,. (1986) Host plant effects on hybrids of Rhizobium leguminosarum biovars viceae and trifoli. Journal of General Microbiology 132, 2063–2070.
16. Skřt, L., Hirsch, P.R,. & Witty, J.F. (1986) Genetic factors in Rhizobium affecting the symbiotic carbon costs of N2 fixation and host biomass production. Journal of Applied Bacteriology 61, 239–246.
17. Hirsch, P.R., Wang, C.L. & Woodward, M.J. (1986) Construction of a Tn5 derivative determining resistance to gentamicin and spectinomycin using a fragment cloned from R1033. Gene 48, 203–209.
18. Wang, C.L. & Hirsch, P.R,. (1988) Mutation, transfer and location of symbiotic genes of Rhizobium leguminosarum biovar phaseoli by insertion of Tn5–mob. Acta Genetica Sinica 15(1), 25–33.
19. Hirsch, P.R,. & Spokes, J.R. (1988) Rhizobium leguminosarum as a model for investigating gene transfer in soil. In: Risk Assessment for Deliberate Releases, ed. Walter Klingmller. Heidelberg: Springer Verlag, pp. 10–17.
20. Hirsch, P.R,. (1988) Assessing the environmental risks of releasing genetically manipulated organisms. In: Science and Change in Agriculture, (J. Hardcastle, Ed.), AFRC.
21. Hirsch, P.R,., Giller, K.E. & Mcgrath, S.P. (1988) Rhizobia isolated from root nodules of clover grown on soils with heavy metal contamination. In Nitrogen Fixation: Hundred Years After (Ed. H. Bothe, F.J. de Bruijn & W.E. Newton). Gustav Fischer, Stuttgart, New York
22. Giller, K.E., Mcgrath, S.P. & Hirsch, P.R. (1988) Suppression of N2–fixation in clover on soil contaminated with heavy metals. In Nitrogen Fixation: Hundred Years After (Ed. H. Bothe, F.J. de Bruijn & W.E. Newton). Gustav Fischer, Stuttgart, New York
23. Mcgrath, S.P., Hirsch, P.R,. & Giller, K.E. (1988) Effect of heavy metal contamination on the genetics of nitrogen–fixing populations of Rhizobium leguminosarum nodulating white clover. In: Environmental Contamination, Venice, (ed. A.A. Orio). C.E.P. Edinburgh.
24. Kahn, D., David, M., Domergue, O., Daveran, M–L., Ghai, J., Hirsch, P.R,. & Batut, J. (1989) Rhizobium meliloti fixGHI sequence predicts involvement of a specific cation pump in symbiotic nitrogen fixation. Journal of Bacteriology 171, 929–939.
25. Giller, K.E., Mcgrath, S.P. & Hirsch, P.R. (1989) Absence of nitrogen fixation in clover grown on soil subject to long–term contamination with heavy metals is due to survival of only ineffective Rhizobium. Soil Biology & Biochemistry 21, 841–848.
26. Hirsch, P.R,. (1990) Past, present and future uses of Rhizobium inoculants. Journal of the Science of Food and Agriculture 50, 130–131.
27. Hirsch, P.R,., O'connell, M., Boistard, P., Puhler, A, & Priefer, U.B. (1990) European Laboratory Without Walls (ELWW) in the field of The Rhizobium-Legume Symbiosis. Paperback 7 pp, ed. A. Vassarotti, Brussels CEC 1990.
28. Hirsch, P.R,. (1990) Factors limiting gene transfer in bacteria. In Bacterial genetics in natural environments. Eds J.C. Fry & M.J. Day, Chapman & Hall, London, 1990.
29. Hirsch, P.R,. & Skinner, F.A. (1992) The identification and classification of Rhizobium and Bradyrhizobium. In Identification Methods in Applied and Environmental Microbiology. Eds R.G. Board, D. Jones & F.A. Skinner. Blackwell Scientific Publications, Oxford, pp. 45-65.
30. Nicholson, P.S., Jones, M.J. & Hirsch, P.R. (1992) Monitoring survival of genetically-modified Rhizobium in the field. In The Release of Genetically Modified Microorganisms. Eds D.E.S. Stewart-Tull & M. Sussman. Plenum Press, New York.
31. Hirsch, P.R,., Jones, M.J., Mcgrath, S.P. & Giller, K.E. (1993) Heavy metals from past applications of sewage sludge decrease the genetic diversity of Rhizobium leguminosarum biovar trifolii populations. Soil Biology. Biochemistry 25, 1485-1490.
32. Hirsch, P.R,. & Spokes, J.D. (1994) Survival and dispersion of genetically modified rhizobia in the field and genetic interactions with native strains. FEMS Microbiology Ecology 15, 147-160.
33. Hirsch, P.R,. (1995) Monitoring genetically modified microorganisms following field release. In: Unanswered safety questions when employing GMOs, CCRO, The Netherlands.
34. Selbitschka, W., Jording, D., Nieman, S., Schmidt, R., Puhler, A., Mendum, T. & Hirsch, P. (1995) Construction and characterization of a Rhizobium leguminosarum biovar viciae strain designed to assess horizontal gene transfer in the environment. FEMS Microbiology Letters 128, 255-263.
35. Hirsch, P.R,. (1995) Detection of microbial DNA sequences by colony hybridization. Molecular Microbial Ecology Manual 2.6.1, 1-12.
36. Hirsch, P.R,. (1996) Potential manipulation of crop rhizosphere. In: Genetic Engineering of Crop Plants for Resistance to Pests and Diseases. Eds. W.S. Pierpoint and P.R. Shewry. British Crop Protection Council.
37. Hirsch, P.R,. (1996) Population dynamics of indigenous and genetically modified rhizobia in the field. New Phytologist 133, 159-171.
38. Arora, D.K., Hirsch, P.R,. & Kerry, B.R. (1996) PCR-based molecular discrimination of Verticillium chlamydosporium isolates. Mycological Research 100, 801-809.
39. Rengel, Z., Gutteridge, R., Hirsch, P., & Hornby, D. (1996) Plant genotype, micronutrient fertilization and take-all infection influence bacterial populations in the rhizosphere of wheat. Plant & Soil 183: 269-277.
40. Phillips, D.A., Joseph, C.M. & Hirsch, P.R. (1997) Occurrence of flavonoids and nucleosides in agricultural soils. Applied and Environmental Microbiology 63: 4573-4577.
41. Rengel, Z., Ross, G. & Hirsch, P. (1998) Colonisation of wheat roots by soil bacteria depends on the plant genotype and micronutrient nutrition. Journal of Plant Nutrition 21: 99-113.
42. Nicholson, P.S. & Hirsch, P.R,. (1998) The effects of pesticides on the diversity of culturable soil bacteria. Journal of Applied Microbiology 84: 551-558.
43. Cullen,D.W. & Hirsch, P.R,. (1998) A simple and rapid method for direct extraction of microbial DNA from soil for PCR. Soil Biology and Biochemistry 30: 983-993.
44. Cullen, D.W., Nicholson, P.S., Mendum, T.A. & Hirsch, P.R. (1998) Monitoring genetically-modified rhizobia in field soils using the polymerase chain reaction. Journal of Applied Microbiology 84:1025-1034.
45. Mendum, T.A., Sockett, R.E. & Hirsch, P.R,. (1998) The detection of Gram-negative bacterial mRNA from soil by RT-PCR FEMS Microbiology Letters 164: 369-373.
46. Lawlor, K., Chaudri, A.M., McGrath, S.P. & Hirsch, P.R. (1999) Gene transfer in bacteria from soils contaminated with heavy metals. Letters in Applied Microbiology 28: 317-320.
47. Mendum, T.A., Sockett, R.E. & Hirsch, P.R,. (1999) Use of molecular and isotopic techniques to monitor the response of autotrophic ammonia-oxidizing populations of the subdivision of the class Proteobacteria in arable soils to nitrogen fertilizer. Applied Environmental Microbiology 65: 4155-4162.
48. Hirsch, P.R,., Mendum, T.A., Pühler,
A. & Selbistchka, W. (2000) The field
release and monitoring of GUS-marked hizobial strain
CT0370. In: Tracking Genetically Engineered Microorganisms: Method Development from Microcosms to the
Field. Eds. J.K. Jansson, J.D. van Elsas & M. Bailey. R.G. Landes Co., Austin, Texas,
49. Hirsch, P.R., Mauchline, T.M., Mendum, T.A & Kerry, B.R. (2000) Detection of the nematophagous Verticillium chlamydosporium in nematode-infested plant roots using PCR. Mycological Research 104: 435-439.
50. Mendum, T.A., Chilima, B.Z. & Hirsch, P.R,. (2000) The PCR amplification of non-tuberculous mycobacterial 16S rRNA sequences from soil. FEMS Microbiological Letters. 185: 189-192.
51. Van Elsas, J.D., Fry, J., Hirsch, P. & Molin, S. (2000) Ecology of plasmid transfer and spread. In: The horizontal gene pool. Ed. C.M. Thomas. Harwood Academic Pubishers, Amsterdam.
52. Lawlor, K., Knight, B.P., Barbosa-Jefferson, V.L., Lane, P.W., Lilley, A.K., Paton, G.I., McGrath, S.P., O’Flaherty, S.M. & Hirsch, P.R,. (2000) Comparison of methods to investigate microbial populations in soils under different agricultural management. FEMS Microbiology Ecology 33, 129-137.
53. Atkins, S. D., Peberdy, J., Kerry, B. R. & Hirsch, P. R. (2000). Development of a transformation system for the root-knot nematode biological control fungus Verticillium chlamydosporium. In: Biology of plant-microbe interactions. Vol. 2 Eds P. J. G. M. de Wit, T. Bisseling & W. J. Stiekema. International Society for Molecular Plant-Microbe Interactions, St Paul.
54. Hirsch, P. R. & Micanovic, D. (2001). Understanding and exploiting interactions between nitrogen-fixing bacteria and plants. In: Genetics and breeding of small grains. Eds S. A. Quarrie, V. Janjic, A. Atanassov, D. Knezevic & S. Stojanovic. ARI-Serbia, Belgrade.
55. O’Flaherty, S., McGrath, S. & Hirsch, P. (2001) Comparison of phenotypic, functional and genetic diversity of bacterial communities in soils. In: Sustainable Management of Soil Organic Matter. Eds. R.M. Rees, B.C. Ball, C.D. Campbell and C.A. Watson. CAB International.
56. Mendum, T.A., Clark, I.M & Hirsch, P.R,. (2001) Characterization of two novel Rhizobium leguminosarum bacteriophages from a field release site of genetically-modified rhizobia. Antonie van Leeuwenhoek 79: 189-197.
57. Hirsch, P.R,., Atkins, S.D., Mauchline, T.H., Morton, C.O., Davies, K.G. & Kerry, B.R. (2001) Methods for studying the nematophagous fungus Verticillium chlamydosporium in the root environment. Plant & Soil 232: 21-30.
58. Powlson, D.S., Hirsch, P.R,. & Brookes, P.C (2001) The role of soil microorganisms in soil organic matter conservation in the tropics. Nutrient Cycling in Agroecosystems 61: 41-51.
59. Brandt L, Feino Cunha J, Weinreich Olsen A, Chilima B, Hirsch P, Appelberg R, Andersen P. (2002) Failure of the Mycobacterium bovis BCG vaccine: some species of environmental mycobacteria block multiplication of BCG and induction of protective immunity to tuberculosis. Infection and Immunity 70: 672-8
60. Mendum, T.A. & Hirsch, P.R,. (2002). Changes in the population structure of beta-group autotrophic ammonia oxidising bacteria in arable soils in response to agricultural practice. Soil Biology Biochemistry 34, 1479-1485.
61. Mauchline, T. H., Kerry, B. R. & Hirsch, P. R. (2002). Quantification in soil and the rhizosphere of the nematophagous fungus Verticillium chlamydosporium by competitive PCR and comparison with selective plating. Applied and Environmental Microbiology 68, 1846-1853.
62. Clark, I. M., Mendum, T. A. & Hirsch, P. R. (2002). The influence of the symbiotic plasmid pRL1J1 on the distribution of GM rhizobia in soil and crop rhizospheres, and implications for gene flow. Antonie van Leeuwenhoek 81, 607-616.
63. Atkins, S.D., Hildago-Diaz, L., Kalisz, H., Mauchline, T.H., Hirsch, P.R,. & Kerry, B.R. (2003) Development of a new management strategy for the control of root-knot nematodes (Meloiogyne spp.) in organic vegetable production. Pest Management Science 59: 183-189.
64. Morton, C. O., Mauchline, T. H., Kerry B. R. & P. R. Hirsch (2003a). PCR-based DNA fingerprinting indicates host related genetic variation in the nematophagous fungus Pochonia chlamydosporia. Mycological Research 107: 198-205.
65. Morton, C. O., Hirsch, P. R., Peberdy, J. P. & Kerry B. R. (2003b). Cloning of and Genetic Variation in the Protease VCP1 from the nematophagous fungus Pochonia chlamydosporia. Mycological Research 107: 38-46.
66. Atkins, S. D., Clark, I. M., Sosnowska, D., Hirsch, P. R. & Kerry, B. R. (2003) Detection and quantification of Plectosphaerella cucumerina , a potential biological control agent of potato cyst nematodes, by using conventional PCR, real-time PCR, selective media, and baiting. Applied and Environmental Microbiology 69, 4788-4793.
67. O'Flaherty, S. M., Hirsch, P. R. & Kerry, B. R. (2003) The influence of the root-knot nematode Meloidogyne incognita , the nematicide aldicarb and the nematophagous fungus Pochonia chlamydosporia on heterotrophic bacteria in soil and the rhizosphere. European Journal of Soil Science 54, 759-766.
68. Atkins S.D., Mauchline, T.H., Kerry, B.R. & Hirsch PR. (2004) Development of a transformation system for the nematophagous fungus Pochonia chlamydosporia. Mycological Research 108, 654-661.
69. Mauchline, T. H., Kerry, B. R. & Hirsch, P. R. (2004) The biocontrol fungus Pochonia chlamydosporia shows nematode host preference at the infraspecific level. Mycological Research 108,161-169.
70. Morton, O.M., Hirsch, P.R,, & Kerry, B.R. (2004) Infection of plant-parasitic nematodes by nematophagous fungi – a review of the application of molecular biology to understand infection processes and to improve biological control. Nematology 6, 161-170.
71. Hirsch, P.R,. (2004) Release of transgenic bacterial inoculants – rhizobia as a case study. Plant & Soil . 266, 1-10.
72. Hirsch, P.R,. & Clark, I.M. (2004) Impact of genetically modified bacterial inoculants on the soil microbial community. In: GM Crops – Ecological Dimensions. Ed. H.F. van Emden & A.J. Gray, pub. AAB, Warwick HRI, Wellesbourne. 141-153.
73. Hirsch, P.R,. (2004) Detection of microbial DNA sequences by colony hybridization. In: Molecular Microbial Ecology Manual 2nd ed, Kowalchuk, G.A.; de Bruijn, F.J.; Head, I.M.; Akkermans, A.D.; van Elsas, J.D. (Eds.). Pub Kluwer Academic Publisher 2.09: 345-356
74. Atkins, S.D., Clark, I.M., Pande, S., Hirsch, P.R,. & Kerry, B.R. (2005) The use of real-time PCR and species-specific primers for the identification and monitoring of Paecilomyces lilacinus FEMS Microbiology Ecology 51, 257-264.
75. Abaye, D.A., Lawlor, K., Hirsch, P.R. & Brookes, P.C. (2005). Changes in the microbial community of an arable soil caused by long-term metal contamination. European Journal of Soil Science 56, 93-102.
Cultured soil bacteria