Applied Microbiology and Biotechnology

, Volume 102, Issue 5, pp 2399–2412 | Cite as

The role of soil bacterial community during winter fallow period in the incidence of tobacco bacterial wilt disease

Environmental biotechnology

Abstract

Bacterial wilt, caused by Ralstonia solanacearum, occurs occasionally during tobacco planting and potentially brings huge economic losses in affected areas. Soil microbes in different management stages play important roles in influencing bacterial wilt incidence. Studies have focused on the impacts of species diversity and composition during cropping periods on disease morbidity; however, the effects of the soil bacterial biomass, species diversity, species succession, and population interactions on morbidity remain unclear during non-cropping periods. In this study, we explored the soil bacterial communities in the non-cropping winter fallow (WF) and cropping late growing (LG) periods under consecutive monoculture systems using 16S ribosomal RNA gene sequencing and qPCR and further analyzed their effects on tobacco bacterial wilt incidence. We found that the bacterial communities in the WF period were significantly different from those in the LG period based on detrended correspondence analysis and dissimilarity tests. Crop morbidity was significantly related to bacterial community structure and to the presence of some genera during WF and LG periods. These genera, such as Arthrobacter, Pseudomonas, Acidobacteria GP6, and Pasteuria, may be potential biological control agents for bacterial wilt. Further analysis indicated that low soil bacterial diversity during the WF period, decrease of bacterial interactions from the WF to LG periods, and low soil biomass during the LG period all have the potential to increase morbidity. In conclusion, an increase of soil bacterial diversity and control of some bacterial abundances in the WF period might be an effective approach in controlling bacterial wilt incidence.

Keywords

Crop morbidity Biological control agents Bacterial interactions Bacterial diversity Bacterial community structure 

Notes

Author contribution

H. Y. and J. L. conceived of the experiment. Y. X. and H. Y. performed the experiment. Y. X. analyzed the data and wrote the manuscript. X. L., D. M., J. T., and Y. G. participated in the discussions.

Compliance with ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interests.

Supplementary material

253_2018_8757_MOESM1_ESM.pdf (2.5 mb)
ESM 1 (PDF 2523 kb)

References

  1. Ahimou F, Deleu MJP (2000) Surfactin and iturin A effects on Bacillus subtilis surface hydrophobicity. Enzym Microb Technol 27(10):749–754.  https://doi.org/10.1016/S0141-0229(00)00295-7 CrossRefGoogle Scholar
  2. Barberán A, Ramirez KS, Leff JW, Bradford MA, Wall DH, Fierer N (2014) Why are some microbes more ubiquitous than others? Predicting the habitat breadth of soil bacteria. Ecol Lett 17(7):794–802.  https://doi.org/10.1111/ele.12282 CrossRefPubMedGoogle Scholar
  3. Berkovitch YA (1996) Instrumentation for plant health and growth in space. Adv Space Res 18(4–5):157–162.  https://doi.org/10.1016/0273-1177(95)00872-C CrossRefPubMedGoogle Scholar
  4. Bramley R, Ellis N, Nable RO, Garside AL (1996) Changes in soil chemical properties under long-term sugar cane monoculture and their possible role in sugar yield decline. Aust J Soil Res 34(6):967–984.  https://doi.org/10.1071/SR9960967 CrossRefGoogle Scholar
  5. Cui P, Fan F, Yin C, Song A, Huang P, Tang Y, Zhu P, Peng C, Li T, Wakelin SA, Liang Y (2016) Long-term organic and inorganic fertilization alters temperature sensitivity of potential N2O emissions and associated microbes. Soil Biol Biochem 93(131–141.  https://doi.org/10.1016/j.soilbio.2015.11.005 CrossRefGoogle Scholar
  6. Defoirdt T, Boon N, Sorgeloos P, Verstraete W, Bossier P (2007) Alternatives to antibiotics to control bacterial infections: luminescent vibriosis in aquaculture as an example. Trends Biotechnol 25(10):472–479.  https://doi.org/10.1128/AEM.01610-13 CrossRefPubMedGoogle Scholar
  7. Deng Y, He Z, Xu M, Qin Y, Van Nostrand JD, Wu L, Roe BA, Wiley G, Hobbie SE, Reich PB (2012a) Elevated carbon dioxide alters the structure of soil microbial communities. Appl Environ Microb 78(8):2991–2995.  https://doi.org/10.1128/AEM.06924-11 CrossRefGoogle Scholar
  8. Deng Y, Jiang YH, Yang Y, He Z, Luo F, Zhou J (2012b) Molecular ecological network analyses. BMC Bioinformatics 13(1):113.  https://doi.org/10.1186/1471-2105-13-113 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461.  https://doi.org/10.1093/bioinformatics/btq461 CrossRefPubMedGoogle Scholar
  10. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200.  https://doi.org/10.1093/bioinformatics/btr381 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. P Nat Acad Sci USA 103(3):626–631.  https://doi.org/10.1073/pnas.0507535103 CrossRefGoogle Scholar
  12. Franke-Whittle IH, Manici LM, Insam H, Stres B (2015) Rhizosphere bacteria and fungi associated with plant growth in soils of three replanted apple orchards. Plant Soil 395(1):317–333.  https://doi.org/10.1007/s11104-015-2562-x CrossRefGoogle Scholar
  13. Franklin RB, Mills AL (2006) Structural and functional responses of a sewage microbial community to dilution-induced reductions in diversity. Microbial Ecol 52(2):280–288.  https://doi.org/10.1007/s00248-006-9033-0 CrossRefGoogle Scholar
  14. Fu L, Penton CR, Ruan Y, Shen Z, Xue C, Li R, Shen Q (2017) Inducing the rhizosphere microbiome by biofertilizer application to suppress banana Fusarium wilt disease. Soil Biol Biochem 104:39–48.  https://doi.org/10.1016/j.soilbio.2016.10.008 CrossRefGoogle Scholar
  15. Garrido P, Gonzalez-Toril E, Garcia-Moyano A, Moreno-Paz M, Amils R, Parro V (2008) An oligonucleotide prokaryotic acidophile microarray: its validation and its use to monitor seasonal variations in extreme acidic environments with total environmental RNA. Environ Microbiol 10(4):836–850.  https://doi.org/10.1111/j.1462-2920.2008.01477.x CrossRefPubMedGoogle Scholar
  16. Granér G, Persson P, Meijer J, Alström S (2003) A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum. FEMS Microbiol Lett 224(2):269–276.  https://doi.org/10.1016/S0378-1097(03)00449-X CrossRefPubMedGoogle Scholar
  17. Hai NV (2015) The use of probiotics in aquaculture. J Appl Microbiol 119(4):917–935.  https://doi.org/10.1111/jam.12886 CrossRefPubMedGoogle Scholar
  18. Handelsman J, Nesmith WC, Raffel SJ (1991) Microassay for biological and chemical control of infection of tobacco by Phytophthora parasitica var. nicotianae. Curr Microbiol 22(5):317–319.  https://doi.org/10.1007/BF02091961 CrossRefGoogle Scholar
  19. Handelsman J, Raffel S, Mester EH, Wunderlich L, Grau CR (1990) Biological control of damping-off of alfalfa seedlings with Bacillus cereus UW85. Appl Environ Microb 56(3):713–718Google Scholar
  20. Hu Y, Wu K, Liu N, Chen H, Jia X (2004) Studies on microbial population dynamics in the cucumber rhizospheres at different developmental stages. Sci Agri Sinica 37(10):1521–1526Google Scholar
  21. Huo Q, Zhang S, Wang R (2007) Advance and control of tobacco bacterial wilt disease. Chin Agri Sci Bull:364–368Google Scholar
  22. Ji G, Wei L, He Y, Wu Y, Bai X (2008) Biological control of rice bacterial blight by Lysobacter antibioticus strain 13-1. Biol Control 45(3):288–296.  https://doi.org/10.1016/j.biocontrol.2008.01.004 CrossRefGoogle Scholar
  23. Johnson PTJ, Preston DL, Hoverman JT, Henderson JS, Paull SH, Richgels KLD, Redmond MD (2012) Species diversity reduces parasite infection through cross-generational effects on host abundance. Ecology 93(1):56–64.  https://doi.org/10.1890/11-0636.1 CrossRefPubMedGoogle Scholar
  24. Kailasapathy K (2002) Microencapsulation of probiotic bacteria: technology and potential applications. Curr Iss Intest Microbiol 3(2):39–48Google Scholar
  25. Kesarcodi-Watson A, Kaspar H, Lategan MJ, Gibson L (2008) Probiotics in aquaculture: the need, principles and mechanisms of action and screening processes. Aquaculture 274(1):1–14.  https://doi.org/10.1016/j.aquaculture.2007.11.019 CrossRefGoogle Scholar
  26. Kloepper JW, Rodríguez-Kábana R, Zehnder AW, Murphy JF, Sikora E, Fernández C (1999) Plant root-bacterial interactions in biological control of soilborne diseases and potential extension to systemic and foliar diseases. Australas Plant Path 28(1):21–26.  https://doi.org/10.1071/AP99003 CrossRefGoogle Scholar
  27. Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Pseudomonas siderophores: a mechanism explaining disease-suppressive soils. Curr Microbiol 4(5):317–320.  https://doi.org/10.1007/BF02602840 CrossRefGoogle Scholar
  28. 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(10):1127–1138.  https://doi.org/10.1038/ismej.2009.61 CrossRefPubMedGoogle Scholar
  29. Lacroix C, Jolles A, Seabloom EW, Power AG, Mitchell CE, Borer ET (2013) Non-random biodiversity loss underlies predictable increases in viral disease prevalence. J Roy Soc Int 11(92):20130947.  https://doi.org/10.1098/rsif.2013.0947 CrossRefGoogle Scholar
  30. Leifert C, Li H, Chidburee S, Hampson S, Workman S, Sigee D, Epton HAS, Harbour A (1995) Antibiotic production and biocontrol activity by Bacillus subtilis CL27 and Bacillus pumilus CL45. J Appl Bacteriol 78(2):97–108.  https://doi.org/10.1111/j.1365-2672.1995.tb02829.x CrossRefPubMedGoogle Scholar
  31. Liu J, Sui Y, Yu Z, Yao Q, Shi Y, Chu H, Jin J, Liu X, Wang G (2016) Diversity and distribution patterns of acidobacterial communities in the black soil zone of northeast China. Soil Biol Biochem 95:212–222.  https://doi.org/10.1016/j.soilbio.2015.12.021 CrossRefGoogle Scholar
  32. Lou L, Qian G, Xie Y, Hang J, Chen H, Zaleta-Rivera K, Li Y, Shen Y, Dussault PH, Liu F (2011) Biosynthesis of HSAF, a tetramic acid-containing macrolactam from Lysobacter enzymogenes. J Am Chem Soc 133(4):643–645.  https://doi.org/10.1021/ja105732c CrossRefPubMedGoogle Scholar
  33. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Ann Rev Microbiol 63(63):541–556.  https://doi.org/10.1146/annurev.micro.62.081307.162918 CrossRefGoogle Scholar
  34. Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P, Dow M, Verdier V, Beer SV, Machado MA (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 13(6):614–629.  https://doi.org/10.1111/j.1364-3703.2012.00804.x CrossRefPubMedGoogle Scholar
  35. Matos A, Kerkhof L, Garland JL (2005) Effects of microbial community diversity on the survival of Pseudomonas aeruginosa in the wheat rhizosphere. Microbial Ecol 49(2):257–264.  https://doi.org/10.1007/s00248-004-0179-3 CrossRefGoogle Scholar
  36. Mazurier S, Corberand T, Lemanceau P, Raaijmakers JM (2009) Phenazine antibiotics produced by fluorescent pseudomonads contribute to natural soil suppressiveness to Fusarium wilt. ISME J 3(8):977–991.  https://doi.org/10.1038/ismej.2009.33 CrossRefPubMedGoogle Scholar
  37. Mengesha WK, Powell SM, Evans KJ, Barry KM (2017) Diverse microbial communities in non-aerated compost teas suppress bacterial wilt. W J Microb Biot 33(3):49.  https://doi.org/10.1007/s11274-017-2212-y CrossRefGoogle Scholar
  38. Moyne AL, Cleveland TE, Tuzun S (2004) Molecular characterization and analysis of the operon encoding the antifungal lipopeptide bacillomycin D. FEMS Microbiol Lett 234(1):43–49.  https://doi.org/10.1111/j.1574-6968.2004.tb09511.x CrossRefPubMedGoogle Scholar
  39. Niu J, Chao J, Xiao Y, Chen W, Zhang C, Liu X, Rang Z, Yin H, Dai L (2017) Insight into the effects of different cropping systems on soil bacterial community and tobacco bacterial wilt rate. J Basic Microbiol 57(1):3–11.  https://doi.org/10.1002/jobm.201600222 CrossRefPubMedGoogle Scholar
  40. Pal KK, Gardener MS (2006) Biological control of plant pathogens. Plant Health Instructor 202:147Google Scholar
  41. Schmidt HP, Kammann C, Niggli C, Evangelou MWH, Mackie KA, Abiven S (2014) Biochar and biochar-compost as soil amendments to a vineyard soil: influences on plant growth, nutrient uptake, plant health and grape quality. Agri Ecosyst Environ 191(117–123.  https://doi.org/10.1016/j.agee.2014.04.001 CrossRefGoogle Scholar
  42. Sharifi-Tehrani A, Zala M, Natsch A, Moënne-Loccoz Y, Défago G (1998) Biocontrol of soil-borne fungal plant diseases by 2,4-diacetylphloroglucinol-producing fluorescent pseudomonads with different restriction profiles of amplified 16S rDNA. Eur J Plant Pathol 104(7):631–643.  https://doi.org/10.1023/A:1008672104562 CrossRefGoogle Scholar
  43. She S, Niu J, Zhang C, Xiao Y, Chen W, Dai L, Liu X, Yin H (2016) Significant relationship between soil bacterial community structure and incidence of bacterial wilt disease under continuous cropping system. Arch Microbiol 199(2):267–275.  https://doi.org/10.1007/s00203-016-1301-x CrossRefPubMedGoogle Scholar
  44. Shen Z, Ruan Y, Xue C, Zhong S, Li R, Shen Q (2015) Soils naturally suppressive to banana Fusarium wilt disease harbor unique bacterial communities. Plant Soil 393(1):1–13.  https://doi.org/10.1007/s11104-015-2474-9 Google Scholar
  45. Shi S, O Callaghan M, Jones EE, Richardson AE, Walter C, Stewart A, Condron L (2012) Investigation of organic anions in tree root exudates and rhizosphere microbial communities using in situ and destructive sampling techniques. Plant Soil 359(359):149–163.  https://doi.org/10.1007/s11104-012-1198-3 CrossRefGoogle Scholar
  46. Shiomi Y, Nishiyama M, Onizuka T, Marumoto T (1999) Comparison of bacterial community structures in the rhizoplane of tomato plants grown in soils suppressive and conducive towards bacterial wilt. Appl Environ Microb 65(9):3996–4001Google Scholar
  47. Silo-Suh LA, Lethbridge BJ, Raffel SJ, He H, Clardy J, Handelsman J (1994) Biological activities of two fungistatic antibiotics produced by Bacillus cereus UW85. Appl Environ Microb 60(6):2023–2030Google Scholar
  48. Smith KP, Havey MJ, Handelsman J (1993) Suppression of cottony leak of cucumber with Bacillus cereus strain UW85. Plant Dis 77(2):139.  https://doi.org/10.1094/PD-77-0139 CrossRefGoogle Scholar
  49. Spence C, Alff E, Johnson C, Ramos C, Donofrio N, Sundaresan V, Bais H (2014) Natural rice rhizospheric microbes suppress rice blast infections. BMC Plant Biol 14(1):130.  https://doi.org/10.1186/1471-2229-14-130 CrossRefPubMedPubMedCentralGoogle Scholar
  50. van Elsas JD, Jansson J, Trevors JT (1997) Modern soil microbiology. Marcel Dekker, New YorkGoogle Scholar
  51. van Elsas JD, Garbeva P, Salles J (2002) Effects of agronomical measures on the microbial diversity of soils as related to the suppression of soil-borne plant pathogens. Biodegradation 13(1):29–40CrossRefPubMedGoogle Scholar
  52. van Elsas JD, Salles JF (2012) Microbial diversity determines the invasion of soil by a bacterial pathogen. P Nat Acad Sci USA 109(4):1159–1164.  https://doi.org/10.1073/pnas.1109326109 CrossRefGoogle Scholar
  53. Voisard C, Keel C, Haas D, Dèfago G (1989) Cyanide production by Pseudomonas fluorescens helps suppress black root rot of tobacco under gnotobiotic conditions. EMBO J 8(2):351–358PubMedPubMedCentralGoogle Scholar
  54. Wagg C, Bender SF, Widmer F, van der Heijden MGA (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. P Nat Acad Sci 111(14):5266–5270.  https://doi.org/10.1073/pnas.1320054111 CrossRefGoogle Scholar
  55. Ward NL, Challacombe JF, Janssen PH, Bernard H, Coutinho PM, Martin W, Gary X, Haft DH, Michelle S, Jonathan B (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microb 75(7):2046–2056.  https://doi.org/10.1128/AEM.02294-08 CrossRefGoogle Scholar
  56. Wu L, Wen C, Qin Y, Yin H, Tu Q, Nostrand JDV, Yuan T, Yuan M, Ye D, Zhou J (2015) Phasing amplicon sequencing on Illumina Miseq for robust environmental microbial community analysis. BMC Microbiol 15(1):1–12.  https://doi.org/10.1186/s12866-015-0450-4 CrossRefGoogle Scholar
  57. Yang H, Niu J, Tao J, Gu Y, Zhang C, She S, Chen W, Yang H, Yin H (2016) The impacts of different green manure on soil microbial communities and crop health. Preprints. doi:  https://doi.org/10.20944/Preprints 2016:2016090056
  58. Yin C, Hulbert SH, Schroeder KL (2013) Role of bacterial communities in the natural suppression of rhizoctonia solani bare patch disease of wheat (Triticum aestivum L.) Appl Environ Microb 79(23):7428–7438.  https://doi.org/10.1128/AEM.01610-13 CrossRefGoogle Scholar
  59. Yin H, Niu J, Ren Y, Cong J, Zhang X, Fan F, Xiao Y, Zhang X, Deng J, Xie M (2015) An integrated insight into the response of sedimentary microbial communities to heavy metal contamination. Sci Rep 5(1):93–102.  https://doi.org/10.1038/srep14266 Google Scholar
  60. Yoshiko I, Masaya N, Shigeto O, Keishi S (2006) Rhizobacterial community-level, sole carbon source utilization pattern affects the delay in the bacterial wilt of tomato grown in rhizobacterial community model system. Appl Soil Ecol 34(1):27–32.  https://doi.org/10.1016/j.apsoil.2005.12.003 CrossRefGoogle Scholar
  61. Zhan F, Lu Y, Guan G (2005) Community structures of microorganisms and their dynamics in the rhizosphere of flue-cured tobacco. Acta Pedol Sin 42(3):488–494Google Scholar
  62. Zhou J, Deng Y, Luo F, He Z, Tu Q, Zhi X (2010) Functional molecular ecological networks. MBio 1(4):e00169-10–e00169-19.  https://doi.org/10.1128/mBio.00169-10 PubMedPubMedCentralGoogle Scholar
  63. Zhou J, Deng Y, Zhang P, Xue K, Liang Y, Van Nostrand JD, Yang Y, He Z, Wu L, Stahl DA (2014) Stochasticity, succession, and environmental perturbations in a fluidic ecosystem. P Nat Acad Sci USA 111(9):836–845.  https://doi.org/10.1073/pnas.1324044111 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.College of Bioscience and Biotechnology and College of AgronomyHunan Agricultural UniversityChangshaChina
  2. 2.School of Minerals Processing and BioengineeringCentral South UniversityChangshaChina

Personalised recommendations