Abstract
Aims
Banana Fusarium wilt disease is caused by the Fusarium oxysporum f. sp. cubense race 4 fungus and is a vast problem for global banana production. Suppressive and conducive soils were analyzed to characterize important microbial populations and soil chemical properties that contribute to disease suppressiveness.
Methods
Soil bacteria communities from the two banana orchards with excellent Fusarium disease suppression (suppressive soil) after long-term monoculture and two adjacent banana orchards with serious Fusarium wilt disease (conducive soils) were compared using deep 16S RNA barcode pyrosequencing.
Result
Compared to the conducive soils within the same field site, higher (P < 0.05) richness and diversity indices were observed in both suppressive soils. Moreover, more operational taxonomic units (OTUs) were observed in the two suppressive soils. Hierarchical cluster analyses showed that bacterial community membership and structure in disease-suppressive soils differed from disease-conducive soils. The Acidobacteria phylum was significantly (P < 0.05) elevated, but Bacteroidetes was significantly (P < 0.05) reduced in suppressive soils. The Gp4, Gp5, Chthonomonas, Pseudomonas, and Tumebacillus genera were significantly (P < 0.05) enriched in suppressive soils, but Gp2 was significantly (P < 0.05) reduced in suppressive soils. Furthermore, the enrichment of Gp5 and Pseudomonas as well as the soil physicochemical properties of available phosphorus were significantly (P < 0.05) correlated with disease suppression.
Conclusions
Naturally disease suppressive soils to banana Fusarium wilt disease harbor unique bacterial communities.
Similar content being viewed by others
References
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
Alabouvette C (1986) Fusarium-wilt suppressive soils from the Châteaurenard region: review of a 10-year study. Agronomie 6:273–284
Alabouvette C (1999) Fusarium wilt suppressive soils: an example of disease-suppressive soils. Australas Plant Pathol 28:57–64
Alabouvette C, Lemanceau P, Steinberg C (1996) Biological control of Fusarium wilts: opportunities for developing a commercial product. In: Hall R (ed) Principles and practice of managing soilborne plant pathogens. APS Press, St Paul, pp 192–212
Amtmann A, Troufflard S, Armengaud P (2008) The effect of potassium nutrition on pest and disease resistance in plants. Physiol Plant 133:682–691
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Baker KF, Cook RJ (1974) Biological control of plant pathogens. WH Freeman, San Francisco, p 433
Berta G, Sampo S, Gamalero E, Massa N, Lemanceau P (2005) Suppression of Rhizoctonia root-rot of tomato by Glomus mossae BEG12 and Pseudomonas fluorescens A6RI is associated with their effect on the pathogen growth and on the root morphogenesis. Eur J Plant Pathol 111:279–288
Biddle JF, Fitz-Gibbon S, Schuster SC, Brenchley JE, House CH (2008) Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment. Proc Natl Acad Sci U S A 105:10583–10588
Bonanomi G, Antignani V, Capodilupo M, Scala F (2010) Identifying the characteristics of organic soil amendments that suppress soilborne plant diseases. Soil Biol Biochem 42:136–144
Bossio DA, Scow KM, Gunapala N, Graham KJ (1998) Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microb Ecol 36:1–12
Boudreau MA, Andrews JH (1987) Factors influencing antagonism of Chaetomium globosum to Venturia inaequalis: a case study in failed biocontrol. Phytopathology 77:1470–1475
Bull CT, Weller DM, Thomashow LS (1991) Relationship between root colonization and suppression of Gaeumannomyces graminis var. tritici by Pseudomonas fluorescens strain 2–79. Phytopathology 81:954–959
Butler D (2013) Fungus threatens top banana. Nature 504:195–196
Buysens S, Heungens K, Poppe J, Hofte M (1996) Involvement of pyochelin and pyoverdin in suppression of Pythium-induced damping-off of tomato by Pseudomonas aeruginosa 7NSK2. Appl Environ Microb 62:865–871
Chauhan R, Maheshwari S, Gandhi S (2000) Effect of nitrogen, phosphorus and farm yard manure levels on stem rot of cauliflower caused by Rhizoctonia solani Kuhn. Agric Sci Dig 20:36–38
Chen YF, Chen W, Huang X, Hu X, Zhao JT, Gong Q, Li XJ, Huang XL (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
Cook RJ, Rovira A (1976) The role of bacteria in the biological control of Gaeumannomyces graminis by suppressive soils. Soil Biol Biochem 8:269–273
Dandurishvili N, Toklikishvili N, Ovadis M, Eliashvili P, Giorgobiani N, Keshelava R, Tediashvili M, Vainstein A, Khmel I, Szegedi E, Chernin L (2011) Broad‐range antagonistic rhizobacteria Pseudomonas fluorescens and Serratia plymuthica suppress Agrobacterium crown gall tumours on tomato plants. J Appl Microbiol 110:341–352
Davey R, McNeill A, Gupta V, Barnett S (2012) Rhizoctonia root rot suppression in an alkaline calcareous soil from a low rainfall farming system. In: Yunusa I (ed) “Capturing opportunities and overcoming obstacles in Australian agronomy”. Proceedings of 16th Australian Agronomy Conference, 14–18 October 2012, Armidale, NSW
de Boer M, Bom P, Kindt F, Keurentjes JJ, van der Sluis I, Van Loon L, Bakker PA (2003) Control of Fusarium wilt of radish by combining Pseudomonas putida strains that have different disease-suppressive mechanisms. Phytopathology 93:626–632
Domínguez J, Negrín M, Rodríguez C (2001) Aggregate water-stability, particle-size and soil solution properties in conducive and suppressive soils to Fusarium wilt of banana from Canary Islands (Spain). Soil Biol Biochem 33:449–455
Domínguez J, Negrín M, Rodríguez C (2003) Evaluating soil sodium indices in soils of volcanic nature conducive or suppressive to Fusarium wilt of banana. Soil Biol Biochem 35:565–575
Etten EV (2005) Multivariate analysis of ecological data using CANOCO. Austral Ecol 30:486–487
Garbeva P, Veen JA, Elsas JD (2004) Assessment of the diversity, and antagonism towards Rhizoctonia solani AG3, of Pseudomonas species in soil from different agricultural regimes. FEMS Microbiol Ecol 47:51–64
Ghorbani R, Wilcockson S, Koocheki A, Leifert C (2008) Soil management for sustainable crop disease control: a review. Environ Chem Lett 6:149–162
Girvan MS, Bullimore J, Pretty JN, Osborn AM, Ball AS (2003) Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Appl Environ Microb 69:1800–1809
Hjort K, Lembke A, Speksnijder A, Smalla K, Jansson JK (2007) Community structure of actively growing bacterial populations in plant pathogen suppressives soil. Microb Ecol 53:399–413
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
Hunter PJ, Petch GM, Calvo-Bado LA, Pettitt TR, Parsons NR, Morgan JAW, Whipps JM (2006) Differences in microbial activity and microbial populations of peat associated with suppression of damping-off disease caused by Pythium sylvaticum. Appl Environ Microb 72:6452–6460
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
Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Pseudomonas siderophores: a mechanism explaining disease-suppressive soils. Curr Microbiol 4:317–320
Kyselková M, Kopecký J, Frapolli M, Défago G, Ságová-Marečková M, Grundmann GL, Moënne-Loccoz Y (2009) Comparison of rhizobacterial community composition in soil suppressive or conducive to tobacco black root rot disease. ISME J 3:1127–1138
Larkin RP, Fravel DR (1998) Efficacy of various fungal and bacterial biocontrol organisms for control of Fusarium wilt of tomato. Plant Dis 82:1022–1028
Lee KCY, Dunfield PF, Morgan XC, Crowe MA, Houghton KM, Vyssotski M, Ryan JL, Lagutin K, McDonald IR, Stott MB (2011) Chthonomonas calidirosea gen. nov., sp. nov., an aerobic, pigmented, thermophilic micro-organism of a novel bacterial class, Chthonomonadetes classis nov., of the newly described phylum Armatimonadetes originally designated candidate division OP10. Int J Syst Evol Microbiol 61:2482–2490
Lemanceau P, Alabouvette C (1993) Suppression of fusarium wilts by fluorescent pseudomonads: mechanisms and applications. Biocontrol Sci Tech 3:219–234
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90
Mazzola M (2002) Mechanisms of natural soil suppressiveness to soilborne diseases. Anton Leeuw Int J G 81:557–564
Meng Q, Yin J, Rosenzweig N, Douches D, Hao JJ (2012) Culture-based assessment of microbial communities in soil suppressive to potato common scab. Plant Dis 96:712–717
Oros-Sichler M, Costa R, Heuer H, Small K (2007) Molecular fingerprinting techniques to analyze soil microbial communities. In: Elsas JV, Jansson J, Trevors J (eds) Modern soil microbiology, 2nd edn. CRC Press, Boca Raton, pp 355–386
Pegg K, Moore N, Bentley S (1996) Fusarium wilt of banana in Australia: a review. Aust J Agr Res 47:637–650
Peng HX, Sivasithamparam K, Turner DW (1999) Chlamydospore germination and Fusarium wilt of banana plantlets in suppressive and conducive soils are affected by physical and chemical factors. Soil Biol Biochem 31:1363–1374
Penton CR, Vadakattu VVSR, Tiedje JM, Ophel-Keller K, Neate SM, Gillings M, Harvey P, Roget DK (2013) Fungal community structure in disease suppressive soils assessed by 28S LSU gene sequencing. PLoS One 9(4), e93893
Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196
Qiu MH, Zhang RF, Xue C, Zhang SS, Li SQ, Zhang N, Shen QR (2012) Application of bio-organic fertilizer can control Fusarium wilt of cucumber plants by regulating microbial community of rhizosphere soil. Biol Fertil Soils 48:807–816
Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ (2011) Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12:38
Roesch LF, Fulthorpe RR, Riva A, Casella G, Hadwin AK, Kent AD, Daroub SH, Camargo FA, Farmerie WG, Triplett EW (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290
Rosenzweig N, Tiedje JM, Quensen JF III, Meng Q, Hao JJ (2012) Microbial communities associated with potato common scab-suppressive soil determined by pyrosequencing analyses. Plant Dis 96:718–725
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
Saravanan T, Muthusamy M, Marimuthu T (2004) Effect of Pseudomonas fluorescens on Fusarium wilt pathogen in banana rhizosphere. J Biol Sci 4:192–198
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 75:7537–7541
Senechkin IV, van Overbeek LS, van Bruggen AH (2014) Greater Fusarium wilt suppression after complex than after simple organic amendments as affected by soil pH, total carbon and ammonia-oxidizing bacteria. Appl Soil Ecol 73:148–155
Shen Z, Zhong S, Wang Y, Wang B, Mei X, Li R, Ruan Y, Shen Q (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
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
Steven B, Chen MQ, Greer CW, Whyte LG, Niederberger TD (2008) Tumebacillus permanentifrigoris gen. nov., sp. nov., an aerobic, spore-forming bacterium isolated from Canadian high Arctic permafrost. Int J Syst Evol Microbiol 58:1497–1501
Tran H, Ficke A, Asiimwe T, Höfte M, Raaijmakers JM (2007) Role of the cyclic lipopeptide massetolide A in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. New Phytol 175:731–742
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
Wang B, Yuan J, Zhang J, Shen Z, Zhang M, Li R, Ruan Y, Shen Q (2013) Effects of novel bioorganic fertilizer produced by Bacillus amyloliquefaciens W19 on antagonism of Fusarium wilt of banana. Biol Fertil Soils 49:435–446
Weller DM (1988) Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annu Rev Phytopathol 26:379–407
Wu TH, Chellemi DO, Graham JH, Martin KJ, Rosskopf EN (2008) Comparison of soil bacterial communities under diverse agricultural land management and crop production practices. Microb Ecol 55:293–310
Xu L, Huang B, Wu Y, Huang Y, Dong T (2011) The cost-benefit analysis for bananas diversity production in China Foc. zones. Am J Plant Sci 2:561–568
Xu M, Chen X, Qiu M, Zeng X, Xu J, Deng D, Sun G, Li X, Guo J (2012) Bar-coded pyrosequencing reveals the responses of PBDE-degrading microbial communities to electron donor amendments. PLoS ONE 7(1), e30439
Zhang F, Zhu Z, Yang X, Ran W, Shen Q (2013) Trichoderma harzianum T-E5 significantly affects cucumber root exudates and fungal community in the cucumber rhizosphere. Appl Soil Ecol 72:41–48
Zhao Q, Dong C, Yang X, Mei X, Ran W, Shen Q, Xu Y (2011) Biocontrol of Fusarium wilt disease for Cucumis melo melon using bio-organic fertilizer. Appl Soil Ecol 47:67–75
Zhao J, Zhang R, Xue C, Xun W, Sun L, Xu Y, Shen Q (2014) Pyrosequencing reveals contrasting soil bacterial diversity and community structure of two main winter wheat cropping systems in China. Microb Ecol 67:443–453
Acknowledgments
This research was supported by the National Key Basic Research Program of China (2015CB150506), the National Natural Science Foundation of China (31372142 and 41101231), the Department of Science and Technology of Hainan Province (ZDZX2013023), the Chinese Ministry of Science and Technology (2013AA102802), the Priority Academic Program Development of the Jiangsu Higher Education Institutions (PAPD), the 111 project (B12009), the Agricultural Ministry of China (201103004), National Key Technology R&D Program of the Ministry of Science and Technology (2011BAD11B03) and the Innovative Research Team Development Plan of the Ministry of Education of China (IRT1256).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Jeff R. Powell .
Zongzhuan Shen and Yunze Ruan contributed equally to this work.
Rights and permissions
About this article
Cite this article
Shen, Z., Ruan, Y., Xue, C. et al. Soils naturally suppressive to banana Fusarium wilt disease harbor unique bacterial communities. Plant Soil 393, 21–33 (2015). https://doi.org/10.1007/s11104-015-2474-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-015-2474-9