Stability and succession of the rhizosphere microbiota depends upon plant type and soil composition

ISME Journal

Volumn 9, Issue 11, 2015, Pages 2349-2359

  Tkacz, Andrzej ^a,b   Cheema, Jitender ^a   Chandra, Govind ^a   Grant, Alastair ^c   Poole, Philip S ^a,b  

^a JOHN INNES CENTRE   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM; CANOLA; COMMUNITY COMPOSITION; COMPOST; DICOTYLEDON; FUNGUS; GRASS; INOCULATION; LEGUME; MICROBIOLOGY; MICROCOSM; RHIZOSPHERE; SAND; SOIL TYPE; SPECIES DIVERSITY; STOCHASTICITY; SUCCESSION; WHEAT;

ARABIDOPSIS; BACTERIA (MICROORGANISMS); BRACHYPODIUM; BRASSICA; MEDICAGO; OLPIDIUM BRASSICAE; PISUM; TRITICUM;

RNA 16S; SOIL;

ARABIDOPSIS; BACTERIUM; BRACHYPODIUM; BRASSICA; CHEMISTRY; CLASSIFICATION; CROP; FUNGUS; MEDICAGO; MICROBIOLOGY; MICROFLORA; PEA; PH; PLANT DEVELOPMENT; RHIZOSPHERE; SOIL; WHEAT;

ARABIDOPSIS; BACTERIA; BRACHYPODIUM; BRASSICA; CROPS, AGRICULTURAL; FUNGI; HYDROGEN-ION CONCENTRATION; MEDICAGO; MICROBIOTA; PEAS; PLANT DEVELOPMENT; RHIZOSPHERE; RNA, RIBOSOMAL, 16S; SOIL; SOIL MICROBIOLOGY; TRITICUM;

EID: 84945472139     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2015.41     Document Type: Article

References (60)

1. Adrangi S, Faramarzi MA, Shahverdi AR, Sepehrizadeh Z. (2010). Purification and characterization of two extracellular endochitinases from Massilia timonae. Carbohydr Res 345: 402-407
2. Bent SJ, Forney LJ. (2008). The tragedy of the uncommon: understanding limitations in the analysis of microbial diversity. ISME J 2: 689-695
3. Berg G, Smalla K. (2009). Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68: 1-13
4. Bertani G. (1951). Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62: 293-300
5. Bodenhausen N, Horton MW, Bergelson J. (2013). Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS One 8: e56329
6. Bressan M, Roncato MA, Bellvert F, Comte G, Haichar FZ, Achouak W, et al. (2009). Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots. ISME J 3: 1243-1257
7. Buee M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, et al. (2009). 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184: 449-456
8. Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, Assenza F, et al. (2012). Revealing structure and assembly cues for Arabidopsis rootinhabiting bacterial microbiota. Nature 488: 91-95
9. Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P. (2013). Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64: 807-838
10. Cardinale M, Brusetti L, Quatrini P, Borin S, Puglia AM, Rizzi A, et al. (2004). Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities. Appl Environ Microbiol 70: 6147-6156
11. Demoling F, Figueroa D, Bååth E. (2007). Comparison of factors limiting bacterial growth in different soils. Soil Biol and Biochem 39: 2485-2495
12. Dennis PG, Miller AJ, Hirsch PR. (2010). Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72: 313-327
13. Edgar RC. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461
14. Eilers KG, Lauber CL, Knight R, Fierer N. (2010). Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biol Biochem 42: 896-903
15. Faramarzi M.A. FM, Tabatabaei Yazdi M, Adrangi S, Jamialahmadi K, Tasharrofi N, Azizmohseni F. (2009). Optimization of cultural condtions for production of chitinase by a soil isolate of Massilia timonae. Biotechnology 8: 99-93
16. Fisher MM, Triplett EW. (1999). Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol 65: 4630-4636
17. Griffiths RI, Whiteley AS, O'Donnell AG, Bailey MJ. (2000). Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNAand rRNA-based microbial community composition. Appl Environ Microbiol 66: 5488-5491
18. Hamady M, Knight R. (2009). Microbial community profiling for human microbiome projects: tools, techniques, and challenges. Genome Res 19: 1141-1152
19. Hamilton MJ, Weingarden AR, Unno T, Khoruts A, Sadowsky MJ. (2013). High-Throughput DNA sequence analysis reveals stable engraftment of gut microbiota following transplantation of previously frozen fecal bacteria. Gut Microbes 4: 125-135
20. Hartwright LM, Hunter PJ, Walsh JA. (2010). A comparison of Olpidium isolates from a range of host plants using internal transcribed spacer sequence analysis and host range studies. Fungal Biol 114: 26-33
21. Hawes MC, Gunawardena U, Miyasaka S, Zhao X. (2000). The role of root border cells in plant defense. Trends Plant Sci 5: 128-133
22. Hilton S, Bennett AJ, Keane G, Bending GD, Chandler D, Stobart R, et al. (2013). Impact of shortened crop rotation of oilseed rape on soil and rhizosphere microbial diversity in relation to yield decline. PLoS One 8: e59859
23. Huson DH, Richter DC, Mitra S, Auch AF, Schuster SC. (2009). Methods for comparative metagenomics. BMC Bioinform 10: S12
24. James TY, Letcher PM, Longcore JE, Mozley-Standridge SE, Porter D, Powell MJ, et al. (2006). A molecular phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). Mycologia 98: 860-871
25. Jones DL, Nguyen C, Finlay RD. (2009). Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321: 5-33
26. Kinkel LL, Bakker MG, Schlatter DC. (2011). A coevolutionary framework for managing diseasesuppressive soils. Annu Rev Phytopathol 49: 47-67
27. Klein E, Ofek M, Katan J, Minz D, Gamliel A. (2013). Soil suppressiveness to fusarium disease shifts in root microbiome associated with reduction of pathogen root colonization. Phytopathology 103: 23-33
28. Knight R, Jansson J, Field D, Fierer N, Desai N, Fuhrman JA, et al. (2012 Unlocking the potential of metagenomics through replicated experimental design. Nat Biotechnol 30: 513-520
29. Lambert B, Meire P, Joos H, Lens P, Swings J. (1990). Fastgrowing, aerobic, heterotrophic bacteria from the rhizosphere of young sugar beet plants. Appl Environ Microbiol 56: 3375-3381
30. Lanfranco L, Young JP. (2012). Genetic and genomic glimpses of the elusive arbuscular mycorrhizal fungi. Curr Opin Plant Biol 15: 454-461
31. Lauber CL, Hamady M, Knight R, Fierer N. (2009). Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75: 5111-5120
32. Lebreton L, Gosme M, Lucas P, Guillerm-Erckelboudt A-Y, Sarniguet A. (2007). Linera relationship bewteen Gaeumannomyces graminis var. tritici (Ggt) gentypic frequencies and diverse severity on wheat roots in the field. Environ Microbiol 9: 492-499
33. Lugtenberg B, Kamilova F. (2009). Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63: 541-556
34. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, et al. (2012). Defining the core Arabidopsis thaliana root microbiome. Nature 488: 86-90
35. Manter DK, Delgado JA, Holm DG, Stong RA. (2010). Pyrosequencing reveals a highly diverse and cultivar-specific bacterial endophyte community in potato roots. Microb Ecol 60: 157-166
36. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JH, et al. (2011). Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332: 1097-1100
37. Murashige T, Skoog F. (1962). A revised medium for rapid growth and bioassays with tobaco tissue cultures. Physiol Plant 15: 473-497
38. Ngugi DK, Stingl U. (2012). Combined analyses of the ITS loci and the corresponding 16 S rRNA genes reveal high micro- and macrodiversity of SAR11 populations in the Red Sea. PLoS One 7: e50274
39. Nuccio EE, Hodge A, Pett-Ridge J, Herman DJ, Weber PK, Firestone MK. (2013). An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. Environ Microbiol 15: 1870-1881
40. O'Reilly T, Niven DF. (1986). Tryptone-yeast extract broth as a culture medium for Haemophilus pleuropneumoniae and Haemophilus parasuis to be used as challenge inocula. Can J Vet Res 50: 441-443
41. Ofek M, Hadar Y, Minz D. (2012). Ecology of root colonizing Massilia (Oxalobacteraceae). PLoS One 7: e40117
42. Osborne CA, Zwart AB, Broadhurst LM, Young AG, Richardson AE. (2011). The influence of sampling strategies and spatial variation on the detected soil bacterial communities under three different landuse types. FEMS Microbiol Ecol 78: 70-79
43. Poole PS, Blyth A, Reid CJ, Walters K. (1994). myo-Inositol catabolism and catabolite regulation in Rhizobium leguminosarum bv. viciae. Microbiology 140: 2787-2795
44. Poole PS, Schofield NA, Reid CJ, Drew EM, Walshaw DL. (1994). Identification of chromosomal genes located downstream of dctD that affect the requirement for calcium and the lipopolysaccharide layer of Rhizobium leguminosarum. Microbiology 140: 2797-2809
45. R Development Core Team. (2008). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, Austria. http://www.R-project.org
46. Sharma S, Aneja MK, Mayer J, Munch JC, Schloter M. (2005). Characterization of bacterial community structure in rhizosphere soil of grain legumes. Microb Ecol 49: 407-415
47. Smith CJ, Danilowicz BS, Clear AK, Costello FJ, Wilson B, Meijer WG. (2005). T-Align, a web-based tool for comparison of multiple terminal restriction fragment length polymorphism profiles. FEMS Microbiol Ecol 54: 375-380
48. Sonderby IE, Hansen BG, Bjarnholt N, Ticconi C, Halkier BA, Kliebenstein DJ. (2007). A systems biology approach identifies a R2R3 MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates. PLoS One 2: e1322
49. Sutherland JP. (1974). Multiple stable states in natural communities. Am Nat 108: 859-873
50. Swenson W, Wilson DS, Elias R. (2000). Artificial ecosystem selection. Proc Natl Acad Sci USA 97: 9110-9114
51. Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, et al. (2009). Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl Environ Microbiol 75: 748-757
52. Terpolilli JJ, Hood GA, Poole PS. (2012). What determines the efficiency of N(2)-fixing Rhizobium-legume symbioses? Adv Microb Physiol 60: 325-389
53. Turner TR, James EK, Poole PS. (2013). The plant microbiome. Genome Biol 14: 209
54. Turner TR, Ramakrishnan K, Walshaw J, Heavens D, Alston M, Swarbreck D, et al. (2013). Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J 7: 2248-2258
55. Udvardi M, Poole PS. (2013). Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64: 781-805
56. Van der Ent S, Van Wees SC, Pieterse CM. (2009). Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70: 1581-1588
57. Wooley JC, Godzik A, Friedberg I. (2010). A primer on metagenomics. PLoS Comput Biol 6: e1000667
58. Wright ES, Yilmaz LS, Noguera DR. (2012). DECIPHER, a search-based approach to chimera identification for 16S rRNA sequences. Appl Environ Microbiol 78: 717-725
59. Yin C, Hulbert SH, Schroeder KL, Mavrodi O, Mavrodi D, Dhingra A, et al. (2013). Role of bacterial communities in the natural suppression of Rhizoctonia solani bare patch disease of wheat (Triticum aestivum L.). Appl Environ Microbiol 79: 7428-7438
60. Yuan H, Ge T, Chen C, O'Donnell AG, Wu J. (2012). Significant role for microbial autotrophy in the sequestration of soil carbon. Appl Environ Microbiol 78: 2328-2336