Deep 16S rRNA pyrosequencing reveals a bacterial community associated with banana Fusarium wilt disease suppression induced by bio-organic fertilizer application

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Shen, Zongzhuan ^a   Wang, Dongsheng ^c   Ruan, Yunze ^b   Xue, Chao ^a   Zhang, Jian ^a   Li, Rong ^a   Shen, Qirong ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b HAINAN UNIVERSITY   (China)

^c Vegetable Science Institute   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; FERTILIZER; NITROGEN; RNA 16S; AMMONIUM DERIVATIVE; SOIL;

ACIDOBACTERIA; ACTINOBACTERIA; ARTICLE; BACTEROIDETES; BANANA; COMMUNITY STRUCTURE; DNA EXTRACTION; FUSARIUM WILT; GEMMATIMONADETE; GENE SEQUENCE; INCIDENCE; MICROBIAL COMMUNITY; MONOCULTURE; NONHUMAN; PROTEOBACTERIA; PYROSEQUENCING; QUALITY CONTROL; SPHINGOMONAS; ANALYSIS OF VARIANCE; BIOLOGY; CHEMISTRY; CHINA; FUSARIUM; GENETICS; HIGH THROUGHPUT SEQUENCING; MICROBIOLOGY; MICROFLORA; MOLECULAR GENETICS; MUSA; NUCLEOTIDE SEQUENCE; ORGANIC FARMING; PLANT DISEASE; PROCEDURES; SOIL; SPECIES DIFFERENCE;

AMMONIUM COMPOUNDS; ANALYSIS OF VARIANCE; BASE SEQUENCE; CHINA; COMPUTATIONAL BIOLOGY; FERTILIZERS; FUSARIUM; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICROBIOTA; MOLECULAR SEQUENCE DATA; MUSA; NITROGEN; ORGANIC AGRICULTURE; PLANT DISEASES; RNA, RIBOSOMAL, 16S; SOIL; SOIL MICROBIOLOGY; SPECIES SPECIFICITY;

EID: 84901611011     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098420     Document Type: Article

References (52)

1. O'Donnell K, Kistler HC, Cigelnik E, Ploetz RC (1998) Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. P Natl Acad Sci USA 95: 2044-2049. (Pubitemid 28145891)
2. Butler D (2013) Fungus threatens top banana. Nature 504: 195-196.
3. Chen YF, Chen W, Huang X, Hu X, Zhao JT, et al. (2013) Fusarium wilt-resistant lines of Brazil banana (Musa spp., AAA) obtained by EMS-induced mutation in a micro-cross-section cultural system. Plant Pathol 62: 112-119.
4. Getha K, Vikineswary S (2002) Antagonistic effects of Streptomyces violaceusniger strain G10 on Fusarium oxysporum f. sp. cubense race 4: Indirect evidence for the role of antibiosis in the antagonistic process. J Ind Microbiol Biot 28: 303-310. (Pubitemid 34753753)
5. Getha K, Vikineswary S, Wong W, Seki T, Ward A, et al. (2005) Evaluation of Streptomyces sp. strain g10 for suppression of Fusarium wilt and rhizosphere colonization in pot-grown banana plantlets. J Ind Microbiol Biot 32: 24-32. (Pubitemid 40486974)
6. Raguchander T, Jayashree K, Samiyappan R (1997) Management of Fusarium wilt of banana using antagonistic microorganisms. J Biol Control 11: 101-105.
7. Saravanan T, Muthusamy M, Marimuthu T (2003) Development of integrated approach to manage the fusarial wilt of banana. Crop Prot 22: 1117-1123. (Pubitemid 37245069)
8. Sivamani E, Gnanamanickam S (1988) Biological control of Fusarium oxysporum f. sp. cubense in banana by inoculation with Pseudomonas fluorescens. Plant Soil 107: 3-9.
9. Wang BB, Yuan J, Zhang J, Shen ZZ, Zhang MX, et al. (2012) Effects of novel bioorganic fertilizer produced by Bacillus amyloliquefaciens W19 on antagonism of Fusarium wilt of banana. Biol Fertil Soils 49: 435-446.
10. El-Hassan S, Gowen S (2006) Formulation and delivery of the bacterial antagonist Bacillus subtilis for management of lentil vascular wilt caused by Fusarium oxysporum f. sp. lentis. J Phytopathol 154: 148-155.
11. Kavino M, Harish S, Kumar N, Saravanakumar D, Samiyappan R (2010) Effect of chitinolytic PGPR on growth, yield and physiological attributes of banana (Musa spp.) under field conditions. Appl Soil Ecol 45: 71-77.
12. Shen ZZ, Zhong ST, Wang YG, Wang BB, Mei XL, et al. (2013) Induced soil microbial suppression of banana fusarium wilt disease using compost and biofertilizers to improve yield and quality. Eur J Soil Biol 57: 1-8.
13. Cotxarrera L, Trillas-Gay MI, Steinberg C, Alabouvette C (2002) Use of sewage sludge compost and Trichoderma asperellum isolates to suppress Fusarium wilt of tomato. Soil Biol Biochem 34: 467-476. (Pubitemid 34315724)
14. Zhao QY, Dong CX, Yang XM, Mei XL, Ran W, et al. (2011) Biocontrol of Fusarium wilt disease for Cucumis melo melon using bio-organic fertilizer. Appl Soil Ecol 47: 67-75.
15. Poulsen PHB, Al-Soud WA, Bergmark L, Magid J, Hansen LH, et al. (2013) Effects of fertilization with urban and agricultural organic wastes in a field trial-Prokaryotic diversity investigated by pyrosequencing. Soil Biol Biochem 57: 784-793.
16. Mazzola M (2004) Assessment and mangement of soil microbial community structre for disease suppression. Annu Rev Phytopathol 42: 35-59.
17. Garbeva P, Van VJ, Van EJ (2004) Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 42: 243-270. (Pubitemid 39308513)
18. Acosta-Martinez V, Dowd S, Sun Y, Allen V (2008) Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biol Biochem 40: 2762-2770.
19. Roesch LF, Fulthorpe RR, Riva A, Casella G, Hadwin AK, et al. (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1: 283-290. (Pubitemid 47227850)
20. Binladen J, Gilbert MTP, Bollback JP, Panitz F, Bendixen C, et al. (2007) The use of coded PCR primers enables high-throughput sequencing of multiple homolog amplification products by 454 parallel sequencing. PLoS One 2: e197.
21. Chen LH, Yang XM, Raza W, Luo J, Zhang FG, et al. (2011) Solid-state fermentation of agro-industrial wastes to produce bioorganic fertilizer for the biocontrol of Fusarium wilt of cucumber in continuously cropped soil. Bioresour Technol 102: 3900-3910.
22. Dethlefsen L, Huse S, Sogin ML, Relman DA (2008) The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16 S rRNA sequencing. PLoS Biol 6: e280.
23. Huse SM, Dethlefsen L, Huber JA, Welch DM, Relman DA, et al. (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4: e1000255.
24. Liu Z, Lozupone C, Hamady M, Bushman FD, Knight R (2007) Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res 35: e120.
25. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 75: 7537-7541.
26. Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ (2011) Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12: 38.
27. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, et al. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
28. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb 73: 5261-5267. (Pubitemid 47326658)
29. Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11: 265-270.
30. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, et al. (2005) Diversity of the human intestinal microbial flora. Science 308: 1635-1638. (Pubitemid 40807514)
31. Washington H (1984) Diversity, biotic and similarity indices: a review with special relevance to aquatic ecosystems. Water Res 18: 653-694.
32. Bunge J, Fitzpatrick M (1993) Estimating the number of species: a review. J Am Stat Assoc 88: 364-373.
33. Warnes GR, Bolker B, Bonebakker L, Gentleman R, Huber W, et al. (2011) gplots: Various R programming tools for plotting data. R package version 2.
34. R Development Core Team (2012) R: A language and environment for statistical computing. Vienna, Austria, http://www.r-project.org.
35. Etten EV (2005) Multivariate analysis of ecological data using CANOCO. Austral Eco 30: 486-487.
36. Chaudhry V, Rehman A, Mishra A, Chauhan PS, Nautiyal CS (2012) Changes in bacterial community structure of agricultural land due to long-term organic and chemical amendments. Microbial Ecol 64: 450-460.
37. Bonanomi G, Antignani V, Pane C, Scala F (2007) Suppression of soilborne fungal diseases with organic amendments. J Plant Pathol 89: 311-324. (Pubitemid 350189205)
38. Qiu MH, Zhang RF, Xue C, Zhang SS, Li SQ, et al. (2012) Application of bio-organic fertilizer can control Fusarium wilt of cucumber plants by regulating microbial community of rhizosphere soil. Biol Fert Soils 48: 807-816.
39. Sun H, Deng S, Raun W (2004) Bacterial community structure and diversity in a century-old manure-treated agroecosystem. Appl Environ Microbiol 70: 5868-5874. (Pubitemid 39471829)
40. 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 Microb 75: 5111-5120.
41. Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, et al. (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4: 1340-1351.
42. Shen CC, Xiong JB, Zhang HY, Feng YZ, Lin XG, et al. (2012) Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57: 204-211.
43. Sanguin H, Sarniguet A, Gazengel K, Moënne-Loccoz Y, Grundmann G (2009) Rhizosphere bacterial communities associated with disease suppressiveness stages of take-all decline in wheat monoculture. New Phytol 184: 694-707.
44. Kyselková M, Kopecký J, Frapolli M, Défago G, Ságová-Marečková M, et al. (2009) Comparison of rhizobacterial community composition in soil suppressive or conducive to tobacco black root rot disease. ISME J 3: 1127-1138.
45. Yin C, Hulbert SH, Schroeder KL, Mavrodi O, Mavrodi D, et al. (2013) Role of bacterial communities in the natural suppression of Rhizoctonia solani bare patch of wheat (Triticum aestivum L.). Appl Environ Microb 79: 7428-7438.
46. Balkwill DL, Fredrickson JK, Romine MF (2006) Sphingomonas and related genera. In Dworkin M, Falkow S, Rosenberg E, Schleifer K, Stackebrandt E, editors. The Prokaryotes: Delta, Epsilon Subclass. Springer, New York. pp. 605-629.
47. Wachowska U, Irzykowski W, Jȩdryczka M, Stasiulewicz-Paluch AD, Głowacka K (2013) Biological control of winter wheat pathogens with the use of antagonistic Sphingomonas bacteria under greenhouse conditions. Biocontrol Sci Tech 23: 1110-1122.
48. Höper H, Alabouvette C (1996) Importance of physical and chemical soil properties in the suppressiveness of soils to plant diseases. Eur J Soil Biol 32: 41-58. (Pubitemid 126828544)
49. Hamel C, Vujanovic V, Jeannotte R, Nakano-Hylander A, St-Arnaud M (2005) Negative feedback on a perennial crop: Fusarium crown and root rot of asparagus is related to changes in soil microbial community structure. Plant Soil 268: 75-87. (Pubitemid 40886238)
50. Pérez-Piqueres A, Edel-Hermann V, Alabouvette C, Steinberg C (2006) Response of soil microbial communities to compost amendments. Soil Biol Biochem 38: 460-470. (Pubitemid 43234190)
51. Mallett K, Maynard D (1998) Armillaria root disease, stand characteristics, and soil properties in young lodgepole pine. Forest Eco Manag 105: 37-44. (Pubitemid 28238608)
52. Oyarzun P, Gerlagh M, Zadoks J (1998) Factors associated with soil receptivity to some fungal root rot pathogens of peas. Appl Soil Ecol 10: 151-169. (Pubitemid 128414814)