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Plant and Soil

, Volume 409, Issue 1–2, pp 329–343 | Cite as

Nutrient use preferences among soil Streptomyces suggest greater resource competition in monoculture than polyculture plant communities

  • Adil Essarioui
  • Harold C. Kistler
  • Linda L. Kinkel
Regular Article

Abstract

Background an aims

Nutrient use overlap among sympatric Streptomyces populations is correlated with pathogen inhibitory capacity, yet there is little information on either the factors that influence nutrient use overlap among coexisting populations or the diversity of nutrient use among soil Streptomyces.

Methods

We examined the effects of plant host and plant species richness on nutrient use of Streptomyces isolated from the rhizosphere of Andropogon gerardii (Ag) and Lespedeza capitata (Lc) growing in communities of 1 (monoculture) or 16 (polyculture) plant species. Growth on 95 carbon sources was assessed over 5d.

Results

Cumulative growth was significantly greater for polyculture vs. monoculture isolates, and for Lc vs. Ag isolates. Isolates from monocultures, but not polycultures, exhibited a drop in growth rates between 24 h and 72 h post-inoculation, suggesting resource allocation to non-growth functions. Isolates from high-carbon (polyculture) or high-nitrogen (Lc) soils had larger niche widths than isolates from low-C (monocultures) or low-N (Ag) soils. Sympatric isolates from polycultures were significantly more differentiated from one another in preferred nutrients for growth than sympatric isolates from monocultures.

Conclusions

These results suggest that Streptomyces populations respond to selection imposed by plant host and plant community richness and that populations from polyculture but not from monoculture, mediate resource competition via niche differentiation.

Keywords

Streptomyces Andropogon gerardii Lespedeza capitata Plant richness 

Notes

Acknowledgments

Adil Essarioui was supported by funds from the Islamic Development Bank. Research was supported by Agricultural and Food Research Grant Initiative Competitive Grant 2011-67019-30200 from the USDA National Institute of Food and Agriculture. Technical and field support from Lindsey Hanson, Dan Schlatter, and Nick LeBlanc were invaluable to completion of the work. Field plots maintained under National Science Foundation Long-Term Ecological Research Grant 0620652 were the source of soil samples used in this study.

Supplementary material

11104_2016_2968_MOESM1_ESM.pdf (278 kb)
ESM 1 (PDF 278 kb)

References

  1. Allison S (2005) Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments. Ecol Lett 8:626–635. doi: 10.1111/j.1461-0248.2005.00756.x CrossRefGoogle Scholar
  2. Badri DV, Vivanco JMJ (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681. doi: 10.1111/j.1365-3040.2009.01926.x CrossRefPubMedGoogle Scholar
  3. Bakker M, Otto-Hanson L, Lange A, Bradeen J, Kinkel L (2013) Plant monocultures produce more antagonistic soil Streptomyces communities than high-diversity plant communities. Soil Biol Biochem 65:304–312. doi: 10.1016/j.soilbio.2013.06.007 CrossRefGoogle Scholar
  4. Becker D, Crockett J (1976) Nitrogen fixation in some prairie legumes. Am Midl Nat 96:133. doi: 10.2307/2424573 CrossRefGoogle Scholar
  5. Becker DM, Kinkel LL (1999) Strategies for quantitative isolation of Streptomyces from soil for studies of pathogen ecology and disease biocontrol. Recent Research Developments in Microbiology 3(1):349–362Google Scholar
  6. Bremer C, Braker G, Matthies D, Beierkuhnlein C, Conrad R (2009) Plant presence and species combination, but not diversity, influence denitrifier activity and the composition of nirK -type denitrifier communities in grassland soil. FEMS Microbiol Ecol 70:377–387. doi: 10.1111/j.1574-6941.2009.00732.x CrossRefPubMedGoogle Scholar
  7. Broeckling C, Broz A, Bergelson J, Manter D, Vivanco J (2007) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744. doi: 10.1128/aem.02188-07 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chen C, Huang C, Lee H, Tsai H, Kirby R (2002) Once the circle has been broken: dynamics and evolution of Streptomyces chromosomes. Trends Genet 18:522–529. doi: 10.1016/s0168-9525(02)02752-x CrossRefPubMedGoogle Scholar
  9. Czàràn T, Hoekstra R, Pagie L (2002) Chemical warfare between microbes promotes biodiversity. Proc Natl Acad Sci 99:786–790. doi: 10.1073/pnas.012399899
  10. Dini-Andreote F, van Elsas J (2013) Back to the basics: the need for ecophysiological insights to enhance our understanding of microbial behaviour in the rhizosphere. Plant Soil 373:1–15. doi: 10.1007/s11104-013-1687-z CrossRefGoogle Scholar
  11. Doumbou C, Hamby Salove M, Crawford D, Beaulieu C (2001) Actinomycetes, promising tools to control plant diseases and to promote plant growth. Phytoprotection 82:85. doi: 10.7202/706219ar
  12. 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 CrossRefGoogle Scholar
  13. Hibbing M, Fuqua C, Parsek M, Peterson S (2009) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8:15–25. doi: 10.1038/nrmicro2259 CrossRefGoogle Scholar
  14. Hirsch A, Bauer W, Bird D, Cullimore J, Tyler B, Yoder J (2003) Molecular signals and receptors: controlling rhizosphere interactions between plants and other organisms. Ecology 84:858–868. doi: 10.1890/0012-9658(2003)084[0858:msarcr]2.0.co;2 CrossRefGoogle Scholar
  15. 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 CrossRefPubMedGoogle Scholar
  16. Kinkel L, Schlatter D, Bakker M, Arenz B (2012) Streptomyces competition and co-evolution in relation to plant disease suppression. Res Microbiol 163:490–499. doi: 10.1016/j.resmic.2012.07.005 CrossRefPubMedGoogle Scholar
  17. Kinkel L, Schlatter D, Xiao K, Baines A (2014) Sympatric inhibition and niche differentiation suggest alternative coevolutionary trajectories among Streptomycetes. ISME J 8:492–492. doi: 10.1038/ismej.2013.213 CrossRefPubMedCentralGoogle Scholar
  18. Kontchou C, Blondeau R (1992) Biodegradation of soil humic acids by Streptomyces viridosporus. Can J Microbiol 38:203–208. doi: 10.1139/m92-034 CrossRefPubMedGoogle Scholar
  19. Lamb E, Kennedy N, Siciliano S (2010) Effects of plant species richness and evenness on soil microbial community diversity and function. Plant Soil 338:483–495. doi: 10.1007/s11104-010-0560-6 CrossRefGoogle Scholar
  20. Langenheder S, Székely AJ (2011) Species sorting and neutral processes are both important during the initial assembly of bacterial communities. The ISME Journal 5:1086–1094. doi: 10.1038/ismej.2010.207
  21. LeBlanc N, Kinkel L, Kistler H (2014) Soil fungal communities respond to grassland plant community richness and soil edaphics. Microb Ecol 70:188–195. doi: 10.1007/s00248-014-0531-1 CrossRefPubMedGoogle Scholar
  22. Li J, Jiao S, Gao R, Bardgett R (2012) Differential effects of legume species on the recovery of soil microbial communities, and carbon and nitrogen contents, in abandoned fields of the loess plateau, China. Environ Manag 50:1193–1203. doi: 10.1007/s00267-012-9958-7 CrossRefGoogle Scholar
  23. Micallef S, Shiaris M, Colon-Carmona A (2009) Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J Exp Bot 60:1729–1742. doi: 10.1093/jxb/erp053 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Nihorimbere V, Ongena M, Smargiassi M, Thonart P (2011) Beneficial effect of the rhizosphere microbial community fpr plant growth and health. Biotechnol Agron Soc Environ 15(2):327–337Google Scholar
  25. Omura S, Ikeda H, Ishikawa J, Hanamoto A, Takahashi C, Shinose M, Takahashi Y, Horikawa H, Nakazawa H, Osonoe T, Kikuchi H, Shiba T, Sakaki Y, Hattori M (2001) Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc Natl Acad Sci 98:12215–12220. doi: 10.1073/pnas.211433198 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Schlatter D, Kinkel L (2014) Global biogeography of Streptomyces antibiotic inhibition, resistance, and resource use. FEMS Microbiol Ecol 88:386–397. doi: 10.1111/1574-6941.12307 CrossRefPubMedGoogle Scholar
  27. Schlatter D, Kinkel L (2015) Do tradeoffs structure antibiotic inhibition, resistance, and resource use among soil-borne Streptomyces? BMC Evol Biol. doi: 10.1186/s12862-015-0470-6
  28. 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 CrossRefPubMedGoogle Scholar
  29. Schlatter D, DavelosBaines A, Xiao K, Kinkel L (2013) Resource use of soil-borne Streptomyces varies with location, phylogeny, and nitrogen amendment. Microb Ecol 66:961–971. doi: 10.1007/s00248-013-0280-6 CrossRefPubMedGoogle Scholar
  30. Seipke R, Kaltenpoth M, Hutchings M (2012) Streptomyces as symbionts: an emerging and widespread theme? FEMS Microbiol Rev 36:862–876. doi: 10.1111/j.1574-6976.2011.00313.x CrossRefPubMedGoogle Scholar
  31. Thonart P, Nihorimbere V, Ongena MM, Smargiassi M (2011) Beneficial effect of the rhizosphere microbial community for plant growth and health Biotechnologie. Agronomie Société et Environnement 15:327–337Google Scholar
  32. Tilman D (2000) Causes, consequences and ethics of biodiversity. Nature 405:208–211. doi: 10.1038/35012217 CrossRefPubMedGoogle Scholar
  33. Tilman D (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845. doi: 10.1126/science.1060391 CrossRefPubMedGoogle Scholar
  34. Vaz Jauri P, Bakker M, Salomon C, Kinkel L (2013) Subinhibitory antibiotic concentrations mediate nutrient use and competition among soil Streptomyces. PLoS One 8:e81064. doi: 10.1371/journal.pone.0081064 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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[0535:pripgv]2.0.co;2 CrossRefGoogle Scholar
  36. Wiggins B, Kinkel L (2005a) Green manures and crop sequences influence alfalfa root rot and pathogen inhibitory activity among soil-borne Streptomycetes. Plant Soil 268:271–283. doi: 10.1007/s11104-004-0300-x CrossRefGoogle Scholar
  37. Wiggins B, Kinkel L (2005b) Green manures and crop sequences influence potato diseases and pathogen inhibitory activity of indigenous Streptomycetes. Phytopathology 95:178–185. doi: 10.1094/phyto-95-0178 CrossRefPubMedGoogle Scholar
  38. Xu W, Deng X, Xu B, Gao Z, Ding W (2014) Photosynthetic activity and efficiency of Bothriochloa ischaemum and Lespedeza davurica in mixtures across growth periods under water stress. Acta Physiol Plant 36:1033–1044. doi: 10.1007/s11738-013-1481-9 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Adil Essarioui
    • 1
    • 2
  • Harold C. Kistler
    • 1
    • 3
  • Linda L. Kinkel
    • 1
  1. 1.Department of Plant PathologyUniversity of MinnesotaSt PaulUSA
  2. 2.Regional Center of ErrachidiaNational Institute of Agronomic ResearchErrachidiaMorocco
  3. 3.Cereal Disease Lab, USDA-ARSSt. PaulUSA

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