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Plant Community Richness Mediates Inhibitory Interactions and Resource Competition between Streptomyces and Fusarium Populations in the Rhizosphere

  • Soil Microbiology
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Abstract

Plant community characteristics impact rhizosphere Streptomyces nutrient competition and antagonistic capacities. However, the effects of Streptomyces on, and their responses to, coexisting microorganisms as a function of plant host or plant species richness have received little attention. In this work, we characterized antagonistic activities and nutrient use among Streptomyces and Fusarium from the rhizosphere of Andropogon gerardii (Ag) and Lespedeza capitata (Lc) plants growing in communities of 1 (monoculture) or 16 (polyculture) plant species. Streptomyces from monoculture were more antagonistic against Fusarium than those from polyculture. In contrast, Fusarium isolates from polyculture had greater inhibitory capacities against Streptomyces than isolates from monoculture. Although Fusarium isolates had on average greater niche widths, the collection of Streptomyces isolates in total used a greater diversity of nutrients for growth. Plant richness, but not plant host, influenced the potential for resource competition between the two taxa. Fusarium isolates had greater niche overlap with Streptomyces in monoculture than polyculture, suggesting greater potential for Fusarium to competitively challenge Streptomyces in monoculture plant communities. In contrast, Streptomyces had greater niche overlap with Fusarium in polyculture than monoculture, suggesting that Fusarium experiences greater resource competition with Streptomyces in polyculture than monoculture. These patterns of competitive and inhibitory phenotypes among Streptomyces and Fusarium populations are consistent with selection for Fusarium-antagonistic Streptomyces populations in the presence of strong Fusarium resource competition in plant monocultures. Similarly, these results suggest selection for Streptomyces-inhibitory Fusarium populations in the presence of strong Streptomyces resource competition in more diverse plant communities. Thus, landscape-scale variation in plant species richness may be critical to mediating the coevolutionary dynamics and selective trajectories for inhibitory and nutrient use phenotypes among Streptomyces and Fusarium populations in soil, with significant implications for microbial community functional characteristics.

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References

  1. Alabouvette C (1986) Fusarium wilt suppressive soils from the Chateaurenard region: review of a 10-year study. Agronomie 6:273–284

    Article  Google Scholar 

  2. Bacon CW, Yates IE (2006) Endophytic root colonization by Fusarium species: histology, plant interactions, and toxicity. Soil Biology 9:133–152

    Article  Google Scholar 

  3. Bakker MG, Otto-Hanson L, Lange AJ, Bradeen J, Kinkel LL (2013) Plant monocultures produce more antagonistic soil Streptomyces communities than high-diversity plant communities. Soil Biol. Biochem. 65:304–312

    Article  CAS  Google Scholar 

  4. Bartelt-Ryser J, Joshi J, Schmid B, Brandl H, Balser T (2005) Soil feedbacks of plant diversity on soil microbial communities and subsequent plant growth. Perspectives in Plant Ecology Evolution and Systematics 7:27–49

    Article  Google Scholar 

  5. Becker DM, Kinkel LL (1999) Strategies for quantitative isolation of Streptomyces from soil for studies of pathogen ecology and disease biocontrol. Rec Res Dev Microbiol 3:349–362

    Google Scholar 

  6. Booth C (1971) The genus Fusarium. England, Commonwealth Mycology Institute, Kew, Surrey, p. 237

    Google Scholar 

  7. Broz A, Broeckling CD, De-la-Peña C, Lewis MR, Greene E, Callaway RM, Sumner LW, Vivanco JM (2010) Plant neighbor identity influences plant biochemistry and physiology related to defense. BMC Plant Biol. 10:115

    Article  PubMed  PubMed Central  Google Scholar 

  8. Burgess LW (1981) General ecology of the fusaria. In: Nelson PE, Toussoun TA, Cook RJ (eds) Fusarium: diseases, biology, and taxonomy. Pennsylvania State University Press, University Park, pp. 225–235

    Google Scholar 

  9. Burgess JG, Jordan EM, Bregu M, Mearns-Spragg A, Boyd KG (1999) Microbial antagonism: a neglected avenue of natural products research. J. Biotechnol. 70(1–3):27–32

    Article  CAS  PubMed  Google Scholar 

  10. Challis GL, Hopwood DA (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite roduction by Streptomyces species. Proc. Nat. Acad. Sci 100:14555e14561

    Article  Google Scholar 

  11. Cragg GM, Grothaus PG, Newman DJ (2009) Impact of natural products on developing new anti-cancer agents. Chem. Rev. 109:3012e3043

    Article  Google Scholar 

  12. Deacon J W (1994) Rhizosphere constraints affecting biocontrol agents applied to seeds. In: seed treatment: prospects and progress. BCPC Monograph 57. Thornton health: British Crop Protection Council, 315–327.

  13. Essarioui A, LeBlanc N, Kistler HC, Kinkel LL (2014) Plant host and community diversity impact the dynamics of resource use by soil Streptomyces. Phytopathology 104(11):38–38 Supplement: 3

  14. Essarioui A, Kistler HC, Kinkel LL (2016) Nutrient use preferences among soil Streptomyces suggest greater resource competition in monoculture than polyculture plant communities. Plant Soil. doi:10.1007/s11104-016-2968-0

    Google Scholar 

  15. Gall LS (1970) Significance of microbial interactions in control of microbial ecosystems. Biotechnol. Bioeng. 12:333–340

    Article  CAS  PubMed  Google Scholar 

  16. Guiot HF (1982) Role of competition for substrate in bacterial antagonism in the gut. Infect. Immun. 38(3):887–892

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Hartmann A, Schmid M, Tuinen D, Berg G (2008) Plant-driven selection of microbes. Plant Soil 321:235–257. doi:10.1007/s11104-008-9814-y

    Article  Google Scholar 

  18. Herr LJ (1959) A method of assaying soils for numbers of actinomycetes antagonistic to fungal pathogens. Phytopathology 49:270–273

    Google Scholar 

  19. Hibbing ME, Fuqua C, Parsek MR, Peterson SB (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat. Rev. Microbiol 81:15–25. doi:10.1038/nrmicro2259

    Article  Google Scholar 

  20. Joshi M, Srivastava R, Sharma AK, Prakash A (2012) Screening of resistant varieties and antagonistic Fusarium oxysporum for biocontrol of Fusarium wilt of chilli. J Plant Pathol Microb 3:134. doi:10.4172/2157-7471.1000134

    Article  Google Scholar 

  21. Kim HS, Park YI (2008) Isolation and identification of a novel microorganism producing the immunosuppressant tacrolimus. J. Biosci. Bioeng. 105:418e421

    Article  Google Scholar 

  22. Kinkel L, Bakker M, Schlatter D (2011) A coevolutionary framework for managing disease-suppressive soils. Annu. Rev. Phytopathol. 49:47–67. doi:10.1146/annurev-phyto-072910-095232

    Article  CAS  PubMed  Google Scholar 

  23. Kinkel LL, Schlatter DC, Bakker MG, Arenz BE (2012) Streptomyces competition and co-evolution in relation to plant disease suppression. Res. Microbiol. 163:490–499

    Article  PubMed  Google Scholar 

  24. Komarova N (2014) Spatial interactions and cooperation can change the speed of evolution of complex phenotypes. Proc. Natl. Acad. Sci. 111:10789–10795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Koskella B, Vos M (2015) Adaptation in natural microbial populations. Annu. Rev. Ecol. Evol. Syst. 46:503–522

    Article  Google Scholar 

  26. Kostrzynska M, Bachand A (2006) Use of microbial antagonism to reduce pathogen levels on produce and meat products: a review. Can. J. Microbiol. 52(11):1017–1026

    Article  CAS  PubMed  Google Scholar 

  27. LeBlanc N, Essarioui A, Kinkel LL, Kistler HC (2014) Fusarium community structure and carbon metabolism phenotypes respond to grassland plant community richness and plant host (abstract). Phytopathology 104(11):67 supplemental 3

    Google Scholar 

  28. Leslie JF, Summerel BA (2006) The Fusarium laboratory manual. Blackwell publishing professional, Iowa-USA

    Book  Google Scholar 

  29. Liu XL, Huang KH, Zhou JZ, Meng L, Wang Y, Zhang LX (2012) Identification and antibacterial characteristics of an endophytic fungus Fusarium oxysporum from Lilium lancifolium. Lett. Appl. Microbiol. 55:399–406

    Article  CAS  PubMed  Google Scholar 

  30. Mazolla M (2004) Assessment and management of soil microbial community structure for disease suppression. Annual Review of Phytopthology 42:35–59

    Article  Google Scholar 

  31. Micallef SA, Shiaris MP, Colon-Carmona A (2009) Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J. Exp. Bot. 60:1729–1742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Moretti AN (2009) Taxonomy of Fusarium genus, a continuous fight between lumpers and splitters. Zbornik Matice srpske za prirodne nauke 117:7–13. doi:10.2298/ZMSPN0917007M

    Article  Google Scholar 

  33. Nelson PE, Toussoun TA, Marasas WFO (1983) Fusarium species: an illustrated manual for identification. Pennsylvania State University Press, University Park, Pennsylvania

    Google Scholar 

  34. O’Brien S, Hodgson D, Buckling A (2013) The interplay between microevolution and community structure in microbial populations. Curr. Opin. Biotechnol. 24:821–825

    Article  PubMed  Google Scholar 

  35. Oksanen J, Blanchet F G, Kindt R, Legendre P, Minchin P R, O’Hara R B, Simpson G L, Solymos P, Stevens M H H, Wagner H (2015) Vegan: community ecology package. http://cran.r-project.org/web/packages/vegan/vegan.pdf.

  36. Schlatter D, Fubuh A, Xiao K, Hernandez D, Hobbie S, Kinkel L (2008) Resource amendments influence density and competitive phenotypes of Streptomyces in soil. Microb. Ecol. 57:413–420. doi:10.1007/s00248-008-9433-4

    Article  PubMed  Google Scholar 

  37. Seipke RF, Kaltenpoth M, Hutchings MI (2011) Streptomyces as symbionts: an emerging and widespread theme? FEMS Microbiol. Rev. 36:862–876

    Article  PubMed  Google Scholar 

  38. Shu RG, Wang FW, Yang YM, Liu YX, Tan RX (2004) Antibacterial and xanthine oxidase inhibitory cerebrosides from Fusarium sp. IFB-121, an endophytic fungus in Quercus variabilis. Lipids 39:667–693

    Article  CAS  PubMed  Google Scholar 

  39. Smith V (2002) Effects of resource supplies on the structure and function of microbial communities. Antonie Van Leeuwenhoek 81:99–106

    Article  CAS  PubMed  Google Scholar 

  40. Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science 2945543:843–845

    Article  Google Scholar 

  41. Tirunarayan MO, Sirsi M (1961) The elaboration of antibacterial substances by Fusarium. Ind. Jour. Med. Res. 49:819–827

    CAS  Google Scholar 

  42. Wardle D, Bonner K, Barker G, Yeates G, Nicholson K, Bardgett R, Watson R, Ghani A (1999) Plant removals in perennial grassland: vegetation dynamics, decomposers, soil biodiversity, and ecosystem properties. Ecol. Monogr. 69:535–568. doi:10.1890/0012-9615(1999)069[535:pripgv]2.0.co;2

  43. Watve MG, Tickoo R, Jog MM, Bhole BD (2001) How many antibiotics are produced by the genus Streptomyces? Arch. Microbiol. 176:386e390

    Article  Google Scholar 

  44. Weibel EK, Hadvary P, Hochuli E, Kupfer E, Lengsfeld H (1987) Lipstatin, an inhibitor of pancreatic lipase, produced by Streptomyces toxytricini. I. Producing organism, fermentation, isolation and biological activity. J. Antibiot 40:1081e1085

    Article  Google Scholar 

  45. Wei-Zhou X, Xi-Ping D, Bing-Cheng X, Zhi-Juan G, Wen-Li D (2014) Photosynthetic activity and efficiency of Bothriochloa ischaemum and Lespedeza davuricain mixtures across growth periods under water stress. Acta Physiol. Plant. 36:1033–1044

    Article  Google Scholar 

  46. West SA, Diggle SP, Buckling A, Gardner A, Griffin AS (2007) The social lives of microbes. Annu. Rev. Ecol. Evol. Syst. 38:53–77

    Article  Google Scholar 

  47. Whipps JM (1997) Developments in the biological control of soil-borne plant pathogens. Adv. Bot. Res. 26:1–134

    Article  Google Scholar 

  48. Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J. Exp. Bot. 52(1):487–511

    Article  CAS  PubMed  Google Scholar 

  49. Wiggins BE, Kinkel LL (2005a) Green manures and crop sequences influence alfalfa root rot and pathogen inhibitory activity among soil-borne Streptomycetes. Plant Soil 268:271–283

    Article  CAS  Google Scholar 

  50. Wiggins BE, Kinkel LL (2005b) Green manures and crop sequences influence potato diseases and pathogen inhibitory activity of indigenous Streptomycetes. Phytopathology 952:178–185

    Article  Google Scholar 

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Acknowledgments

We thank the Cedar Creek Ecosystem Science Reserve for permission to collect soil samples. We also thank the staff in our lab, including especially Lindsey Hanson, for their help and feedback to improve this work.

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Authors and Affiliations

  1. Department of Plant Pathology, University of Minnesota, Minneapolis, MN, USA

    Adil Essarioui, Nicholas LeBlanc, Harold C. Kistler & Linda L. Kinkel

  2. National Institute of Agronomic Research, Regional Center of Errachidia, Errachidia, Morocco

    Adil Essarioui

  3. Cereal Disease Lab, USDA-ARS, 1551 Lindig Street, St Paul, MN, USA

    Harold C. Kistler

Authors
  1. Adil Essarioui
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  2. Nicholas LeBlanc
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  3. Harold C. Kistler
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  4. Linda L. Kinkel
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Correspondence to Adil Essarioui.

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Essarioui, A., LeBlanc, N., Kistler, H.C. et al. Plant Community Richness Mediates Inhibitory Interactions and Resource Competition between Streptomyces and Fusarium Populations in the Rhizosphere. Microb Ecol 74, 157–167 (2017). https://doi.org/10.1007/s00248-016-0907-5

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  • DOI: https://doi.org/10.1007/s00248-016-0907-5

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