Skip to main content

Advertisement

SpringerLink
Log in

Densities and inhibitory phenotypes among indigenous Streptomyces spp. vary across native and agricultural habitats

  • Soil Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Streptomyces spp. perform vital roles in natural and agricultural soil ecosystems including in decomposition and nutrient cycling, promotion of plant growth and fitness, and plant disease suppression. Streptomyces densities can vary across the landscape, and inhibitory phenotypes are often a result of selection mediated by microbial competitive interactions in soil communities. Diverse environmental factors, including those specific to habitat, are likely to determine microbial densities in the soil and the outcomes of microbial species interactions. Here, we characterized indigenous Streptomyces densities and inhibitory phenotypes from soil samples (n = 82) collected in 6 distinct habitats across the Cedar Creek Ecosystem Science Reserve (CCESR; agricultural, prairie, savanna, wetland, wet-woodland, and forest). Significant variation in Streptomyces density and the frequency of antagonistic Streptomyces were observed among habitats. There was also significant variation in soil chemical properties among habitats, including percent carbon, percent nitrogen, available phosphorus, extractable potassium, and pH. Density and frequency of antagonists were significantly correlated with one or more environmental parameters across all habitats, though relationships with some parameters differed among habitats. In addition, we found that habitat rather than spatial proximity was a better predictor of variation in Streptomyces density and inhibitory phenotypes. Moreover, habitats least conducive for Streptomyces growth and proliferation, as determined by population density, had increased frequencies of inhibitory phenotypes. Identifying environmental parameters that structure variation in density and frequency of antagonistic Streptomyces can provide insight for determining factors that mediate selection for inhibitory phenotypes across the landscape.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Manivasagan P, Venkatesan J, Sivakumar K, Kim SK (2015) Marine actinobacterial metabolites and their pharmaceutical potential. In: Kim SK (ed) Springer handbook of marine biotechnology. Springer, Berlin, Heidelberg, pp 1371–1386. https://doi.org/10.1007/978-3-642-53971-8_63

    Chapter  Google Scholar 

  2. Zothanpuia PAK, Leo VV, Chandra P, Kumar B, Nayak C, Hashem A, Abd Allah EF, Alqarawi AA, Singh BP (2018) Bioprospection of actinobacteria derived from freshwater sediments for the potential to produce antimicrobial compounds. Microb Cell Factories 17:68. https://doi.org/10.1186/s12934-018-0912-0

    Article  CAS  Google Scholar 

  3. Sarmiento-Vizcaíno A, Braña AF, González V, Herminio N, Molina A, Llera E, Fiedler H-P, Rico JM, García-Flórez L, Acuña JL, García LA, Blanco G (2016) Atomospheric dispersal of bioactive Streptomyces albidoflavus strains among terrestrial and marine environments. Microb Ecol 71:375–386. https://doi.org/10.1007/s00248-015-0654-z

    Article  PubMed  Google Scholar 

  4. Otto-Hanson LK, Grabau Z, Rosen C, Salomon CE, Kinkel LL (2013) Pathogen variation and urea influence selection and success of Streptomyces mixtures in biological control. Phytopathol 103(1):34–42. https://doi.org/10.1094/PHYTO-06-12-0129-R

    Article  CAS  Google Scholar 

  5. Cao P, Liu CX, Su PY, Fu XP, Wang SX, Wu FZ, Wang XJ (2016) An endophytic Streptomyces sp. strain DHV3-2 from diseased root as a potential biocontrol agent against Verticillium dahiae and growth elicitor in tomato (Solanum lycopersicum). Antonie Van Leeuwenhoek 109(12):1573–1582. https://doi.org/10.1007/s10482-016-0758-6

    Article  CAS  PubMed  Google Scholar 

  6. Kunova A, Bonaldi M, Saracchi M, Pizzatti C, Chen XL, Cortesi P (2016) Selection of Streptomyces against soil borne fungal pathogens by a standardized dual culture assay and evaluation of their effects on seed germination and plant growth. BMC Microbiol 16:272. https://doi.org/10.1186/s12866-016-0886-1

    Article  PubMed  PubMed Central  Google Scholar 

  7. Kumbhar C, Mudliar P, Bhatia L, Kshirsagar A, Watve M (2014) Widespread predatory abilities in the genus Streptomyces. Arch Microbiol 196:235–248. https://doi.org/10.1007/s00203-014-0961-7

    Article  CAS  PubMed  Google Scholar 

  8. Findlay BL (2016) The chemical ecology of predatory soil bacteria. ACS Chem Biol 11(6):1502–1510. https://doi.org/10.1021/acschembio.6b00176

    Article  CAS  PubMed  Google Scholar 

  9. Loria R, Bignell DRD, Moll S, Huguet-Tapia JC, Joshi MV, Johnson EG, Seipke RF, Gibson DM (2008) Thaxtomin biosynthesis: the path to plant pathogenicity in the genus Streptomyces. Antonie Leeuwenhoek 94:3–10. https://doi.org/10.1007/s10482-008-9240-4

    Article  PubMed  Google Scholar 

  10. Beaulieu C, Sidibe A, Jabloune R, Simao-Beaunoir AM, Lerat S, Monga E, Bernards MA (2016) Physical, chemical, and proteomic evidence of potato suberin degradation by the plant pathogenic bacteria Streptomyces scabiei. Microbes Environ 31(4):427–434. https://doi.org/10.1264/jsme2.ME16110

    Article  PubMed  PubMed Central  Google Scholar 

  11. Jourdan S, Francis IM, Deflandre B, Loria R, Rigali S (2017) Tracking the subtle mutations driving host sensing by the plant pathogen Streptomyces scabies. mSphere 2:e00367–e00316. https://doi.org/10.1128/mSphere.00367-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Maruna M, Sturdikova M, Liptaj T, Godany A, Muckova M, Certik M, Pronayova N, Proksa B (2010) Isolation, structure elucidation and biological activity of angucycline antibiotics from an epiphytic yew. J Basic Microbiol 50(2):135–142. https://doi.org/10.1002/jobm.200900227

    Article  CAS  PubMed  Google Scholar 

  13. West ER, Cother EJ, Steel CC, Ash GJ (2010) The characterization and diversity of bacterial endophytes of grapevine. Can J Microbiol 56:209–216. https://doi.org/10.1139/w10-004

    Article  CAS  PubMed  Google Scholar 

  14. Salam N, Khieu TN, Liu MJ, Vu TT, Chu-Ky S, Quach NT, Phi QT, Rao MPN, Fontana A, Sarter S, Li WJ (2017) Endophytic Actinobacteria associated with Dracaena cochinchinensis Lour: isolation, diversity, and their cytotoxic activities. Biomed Res Int 1308563. https://doi.org/10.1155/2017/1308563

  15. Zin NM, Baba MS, Zainal-Abidin AH, Latip J, Mazlan NW, Edrada-Ebel R (2017) Gancidin W, a potential low-toxicity antimalarial agent isolated from an endophytic Streptomyces SUK10. Drug Design Dev Therapy 11:351–363. https://doi.org/10.2147/DDDT.S121283

    Article  CAS  Google Scholar 

  16. Garda AL, Fernández-Abalos JM, Sánchez P, Ruiz-Arribas A, Santamaria RI (1997) Two genes encoding an endoglucanase and cellulose-binding protein are clustered and co-regulated by a TTA codon in Streptomyces halstedii JM8. Biochem J 324:403–411. https://doi.org/10.1042/bj3240403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Da Vinha FNM, Gravina-Oliveira MP, Franco MN, Macrae A, Bon EPD, Nascimento RP, Coelho RRR (2011) Cellulase production by Streptomyces viridobrunneus SCPE-09 using lignocellulosic biomass as inducer substrate. Appl Biochem Biotechnol 164(3):256–267. https://doi.org/10.1007/s12010-010-9132-8

    Article  CAS  PubMed  Google Scholar 

  18. Takasuka TE, Book AJ, Lewin GR, Currie CR, Fox BG (2013) Aerobic deconstruction of cellulosic biomass by an insect-associated Streptomyces. Sci Rep 3:1030. https://doi.org/10.1038/srep01030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Book AJ, Lewin GR, McDonald BR, Takasuka TE, Wendt-Pienkowski E, Doering DT, Suh S, Raffa KF, Fox BG, Currie CR (2016) Evolution of high cellulolytic activity in symbiotic Streptomyces through selection of expanded gene content and coordinated gene expression. PLoS Biol 14(6):e1002475. https://doi.org/10.1371/journal.pbio.1002475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Vaz Jauri P, Altier N, Kinkel LL (2016) Streptomyces for sustainability. In: Castro-Sowinski S (ed) Microbial models: from environmental to industrial sustainability. Springer Singapore, Singapore, pp 251–276. https://doi.org/10.1007/978-981-10-2555-6_12

    Chapter  Google Scholar 

  21. Alvarez A, Saez JM, Davila Costa JS, Colin VL, Fuentes MS, Cuozzo SA, Benimeli CS, Polti MA, Amoroso MJ (2017) Actinobacteria: current research and perspectives for bioremediation of pesticides and heavy metals. Chemosphere 166:41–62. https://doi.org/10.1016/j.chemosphere.2016.09.070

    Article  CAS  PubMed  Google Scholar 

  22. Fuentes MS, Raimondo EE, Amoroso MJ, Benimeli CS (2017) Removal of a mixture of pesticides by a Streptomyces consortium: influence of different soil systems. Chemosphere 173:359–367. https://doi.org/10.1016/j.chemosphere.2017.01.044

    Article  CAS  PubMed  Google Scholar 

  23. Kruasuwan W, Thamchaipenet A (2016) Diversity of culturable plant-growth promoting bacterial endophytes associated with sugarcane roots and their effect of growth by co-inoculation of diazotrophs and actinomycetes. J Plant Growth Regul 35(4):1074–1087. https://doi.org/10.1007/s00344-016-9604-3

    Article  CAS  Google Scholar 

  24. Passari AK, Chandra P, Zothanpuia MVK, Leo VV, Gupta VK, Kumar B, Singh BP (2016) Detection of biosynthetic gene and phytohormone production by endophytic actinobacteria associated with Solanum lycopersicum and their plant-growth-promoting effect. Res Microbiol 167(8):692–705. https://doi.org/10.1016/j.resmic.2016.07.001

    Article  CAS  PubMed  Google Scholar 

  25. Das G, Patra JK, Baek KH (2017) Antibacterial properties of endophytic bacteria isolated from a fern species Equisetum arvense L. against foodborne pathogenic bacteria Staphylococcus aureus and Escherichia coli O157:H7. Foodborne Pathog Dis 14(1):50–58. https://doi.org/10.1089/fpd.2016.2192

    Article  CAS  PubMed  Google Scholar 

  26. Liu DQ, Anderson NA, Kinkel L (1996) Selection and characterization of strains of Streptomyces suppressive to the potato scab pathogen. Can J Microbiol 42(5):487–502. https://doi.org/10.1139/m96-066

    Article  Google Scholar 

  27. Xiao K, Kinkel LL, Samac DA (2002) Biological control of Phytophthora root rots on alfalfa and soybean with Streptomyces. Biol Control 23(3):285–295. https://doi.org/10.1080/09583150410001665187

    Article  CAS  Google Scholar 

  28. Ryan AD, Kinkel LL, Schottel JL (2004) Effect of pathogen isolate, potato cultivar, and antagonist strain on potato scab severity and biological control. Biocontrol Sci Tech 14(3):301–311. https://doi.org/10.1080/09583150410001665187

    Article  Google Scholar 

  29. Ma Z, Liu JX, Shentu XP, Bian YL, Yu XP (2014) Optimization of electroporation conditions for toyocamycin producer Streptomyces diastatochromogenes 1628. J Basic Microbiol 54(4):278–284. https://doi.org/10.1002/jobm.201200489

    Article  CAS  PubMed  Google Scholar 

  30. Nagpure A, Choudhary B, Kumar S, Gupta RK (2014) Isolation and characterization of chitinolytic Streptomyces sp. MT7 and its antagonism towards wood-rotting fungi. Ann Microbiol 64(2):531–541. https://doi.org/10.1007/s13213-013-0686-x

    Article  CAS  Google Scholar 

  31. Cordovez V, Carrion VJ, Etalo DW, Mumm R, Zhu H, van Wezel GP, Raaijmakers JM (2015) Diversity and functions of volatile organic compounds produced by Streptomyces from a disease-suppressive soil. Front Microbiol 6:1081. https://doi.org/10.3389/fmicb.2015.01081

    Article  PubMed  PubMed Central  Google Scholar 

  32. Cumsille A, Undabarrena A, Gonzalez V, Claverias F, Rojas C, Camara B (2017) Biodiversity of actinobacteria from the South Pacific and the assessment of Streptomyces chemical diversity with metabolic profiling. Marine Drugs 15(9):286. https://doi.org/10.3390/md15090286

    Article  CAS  PubMed Central  Google Scholar 

  33. Hussain A, Rather MA, Shah AM, Bhat ZS, Shah A, Ahmad Z, Hassan QP (2017) Antituberculotic activity of actinobacteria isolated from the rare habitats. Lett Appl Microbiol 65(3):256–264. https://doi.org/10.1111/lam.12773

    Article  CAS  PubMed  Google Scholar 

  34. Rasuk MC, Ferrer GM, Kurth D, Portero LR, Farias ME, Albarracin VH (2017) UV-resistant actinobacteria from high-altitude Andean lakes: isolation, characterization, and antagonistic activities. Photochem Photobiol 93(3):865–880. https://doi.org/10.1111/php.12759

    Article  CAS  PubMed  Google Scholar 

  35. Mohammadipanah F, Wink J (2016) Actinobacteria from arid and desert habitats: diversity and biological activity. Front Microbiol 6:1541. https://doi.org/10.3389/fmicb.2015.01541

    Article  PubMed  PubMed Central  Google Scholar 

  36. Suriya J, Bharathiraja S, Manivasagan P, Kim SK (2016) Enzymes from rare actinobacterial strains. Advances in Food and Nutrition Research: Marine Enzymes Biotechnology: Production and Industrial Applications, Pt II-Marine Organisms Producing Enzymes 79:67–98. https://doi.org/10.1016/bs.afnr.2016.08.002

    Article  CAS  Google Scholar 

  37. Sanjenbam P, Kannabiran K (2016) Bioactivity of Pyrrolo[1,2-a]pyrazine-1,4-dione, hexahydro-3-(phenylmethyl)-extracted from Streptomyces sp. VITPK9 isolated from the salt spring habitat of Manipur, India. Asian J Pharmaceutics 10(4):265–270. https://doi.org/10.22377/ajp.v10i04.865

    Article  CAS  Google Scholar 

  38. Encheva-Malinova M, Stoyanova M, Avranova H, Pavlova Y, Gocheva B, Ivanova I, Moncheva P (2014) Antibacterial potential of streptomycete strains from Antarctic soils. Biotechnol Biotechnol Equip 28(4):721–727. https://doi.org/10.1080/13102818.2014.947066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Smanski MJ, Schlatter DC, Kinkel LL (2016) Leveraging ecological theory to guide natural product discovery. J Ind Microbiol Biotechnol 43:115. https://doi.org/10.1007/s10295-015-1683-9

    Article  CAS  PubMed  Google Scholar 

  40. Behie SW, Bonet B, Zacharia VM, McClung DJ, Traxler MF (2017) Molecules to ecosystems: actinomycete natural products in situ. Front Microbiol 7:2149. https://doi.org/10.3389/fmicb.2016.02149

    Article  PubMed  PubMed Central  Google Scholar 

  41. Tyc O, Song C, Dickschat JS, Vos M, Garbeva P (2017) The ecological role of volatile and soluble secondary metabolites produced by soil bacteria. Trends Microbiol 25(4):280–292. https://doi.org/10.1016/j.tim.2016.12.002

    Article  CAS  PubMed  Google Scholar 

  42. van der Meij A, Worsley SF, Hutchings MI, van Wezel GP (2017) Chemical ecology of antibiotic production by actinomycetes. FEMS Microbiol Rev 41(3):392–416. https://doi.org/10.1093/femsre/fux005

    Article  CAS  PubMed  Google Scholar 

  43. Garbeva P, Van Veen JA, Van Elsas JD (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. https://doi.org/10.1146/annurev.phyto.42.012604.135455

    Article  CAS  PubMed  Google Scholar 

  44. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. P Natl Acad Sci USA 103:626–631. https://doi.org/10.1073/pnas.0507535103

    Article  CAS  Google Scholar 

  45. Garbeva P, Van Elsas JD, Van Venn JA (2008) Rhizosphere microbial community and its response to plant species and soil history. Plant Soil 302:19–32. https://doi.org/10.1007/s11104-007-9432-0

    Article  CAS  Google Scholar 

  46. Lauber C, 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 Microbiol 75:5111–5120. https://doi.org/10.1128/AEM.00335-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Griffiths RI, Thomson BC, James P, Bell T, Bailey M, Whiteley AS (2011) The bacterial biogeography of British soils. Environ Microbiol 13:1642–1654. https://doi.org/10.1111/j.1462-2920.2011.02480.x

    Article  PubMed  Google Scholar 

  48. Andam CP, Doroghazi JR, Campbell AN, Kelly PJ, Choudoir MJ, Buckley DH (2016) A latitudinal diversity gradient in terrestrial bacteria of the genus Streptomyces. mBio 7(2):e02200–e02215. https://doi.org/10.1128/mBio.02200-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Choudoir MJ, Doroghazi JR, Buckley DH (2016) Latitude delineates patterns of biogeography in terrestrial Streptomyces. Environ Microbiol 18(12):4931–4945. https://doi.org/10.1111/1462-2920.13420

    Article  PubMed  Google Scholar 

  50. Becklund KK, Kinkel LL, Powers JS (2014) Landscape-scale variation in pathogen-suppressive bacteria in tropical dry forest soils of Costa Rica. Biotropica 46(6):657–666. https://doi.org/10.1111/btp.12155

    Article  Google Scholar 

  51. Schlatter DC, Kinkel LL (2014) Global biogeography of Streptomyces antibiotic inhibition, resistance, and resource use. FEMS Microbiol Ecol 88:386–397. https://doi.org/10.1111/1574-6941.12307

    Article  CAS  PubMed  Google Scholar 

  52. Kim BS, Lee JY, Hwang BK (1998) Diversity of actinomycetes antagonisitic to plant pathogenic fungi in cave and sea-mud soils of Korea. J Microbiol 36(2):86–92

    Google Scholar 

  53. Mason CJ, Zeldin EL, Currie CR, Raffa KF, McCrown BH (2014) Populations of uncultivated American cranberry in sphagnum bog communities harbor novel assemblages of actinobacteria with antifungal properties. Botany 92(8):589–595. https://doi.org/10.1139/cjb-2014-0025

    Article  Google Scholar 

  54. Bakker MG, Otto-Hanson LK, Lange AJ, Bradeen JM, Kinkel LL (2013) Plant monocultures produce more antagonistic soil Streptomyces communities than high-diversity plant communities. Soil Biol Biochm 65:304–312. https://doi.org/10.1016/j.soilbio.2013.06.007

    Article  CAS  Google Scholar 

  55. Essarioui A, LeBlanc N, Kistler HC, Kinkel LL (2017) Plant community richness mediates inhibitory interactions and resource competition between Streptomyces and Fusarium populations in the rhizosphere. Microb Ecol 74:157–167. https://doi.org/10.1007/s00248-016-0907-5

    Article  PubMed  Google Scholar 

  56. D’Costa VM, McGrann KM, Hughes DW, Wright GD (2006) Sampling the antibiotic resistome. Science 311:374–377. https://doi.org/10.1126/science.1120800

    Article  PubMed  Google Scholar 

  57. Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J (2010) Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol 8(4):251–259. https://doi.org/10.1038/nrmicro2312

    Article  CAS  PubMed  Google Scholar 

  58. Gibson MK, Forsberg KJ, Dantas G (2015) Improved annotation of antibiotic resistance determinants reveals microbial resistome cluster by ecology. ISME J 9(1):207–216. https://doi.org/10.1038/ismej.2014.106

    Article  CAS  PubMed  Google Scholar 

  59. Schlatter DC, Kinkel LL (2015) Do tradeoffs structure antibiotic inhibition, resistance, and resource use among soil-borne Streptomyces? BMC Evol Biol 15:186. https://doi.org/10.1186/s12862-015-0470-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Davelos AL, Xiao K, Flor JM, Kinkel LL (2004) Genetic and phenotypic traits of streptomycetes used to characterize antibiotic activities of field-collected microbes. Can J Microbiol 50:79–89. https://doi.org/10.1139/w03-107

    Article  CAS  PubMed  Google Scholar 

  61. Davelos AL, Xiao K, Samac DA, Martin AP, Kinkel LL (2004) Spatial variation in Streptomyces genetic composition and diversity in prairie soil. Microb Ecol 48:601–612. https://doi.org/10.1007/s00248-004-0031-9

    Article  CAS  PubMed  Google Scholar 

  62. Saadoun I, Wahiby L, Ababneh Q, Jaradat Z, Massadeh M, Al Momani F (2008) Recovery of soil streptomycetes from arid habitats in Jordan and their potential to inhibit multi-drug resistant Pseudomonas aeruginosa pathogens. World J Microbial Biotechnol 24(2):157–162. https://doi.org/10.1007/s11274-007-9451-2

    Article  CAS  Google Scholar 

  63. Patil HJ, Srivastava AK, Kumar S, Chaudhari BL, Arora DK (2010) Selective isolation, evaluation and characterization of antagonistic actinomycetes against Rhizoctonia solani. World J Microbiol Biotechnol. https://doi.org/10.1007/s11274-010-0400-0

  64. Kanini GS, Katsifas EA, Savvides AL, Hatzinikolaou DG, Karagouni AD (2013) Greek indigenous strepotmycetes as biocontrol agents against the soil-borne fungal plant pathogen Rhizoctonia solani. J Appl Microbiol 114(5):1468–1479. https://doi.org/10.1111/jam.12138

    Article  CAS  PubMed  Google Scholar 

  65. Kinkel LL, Schlatter DC, Xiao K, Baines AD (2014) Sympatric inhibition and niche differentiation suggest alternative coevolutionary trajectories among streptomycetes. ISME J 8(2):249–256. https://doi.org/10.1038/ismej.2013.175

    Article  CAS  PubMed  Google Scholar 

  66. Schlatter DC, Bakker MG, Bradeen JM, Kinkel LL (2015) Plant community richness and microbial interactions structure bacterial communities in soil. ECOL 96(1):134–142. https://doi.org/10.1890/13-1648.1

    Article  Google Scholar 

  67. Schlatter DC, Fubuh A, Xiao K, Hernandez D, Hobbie S, Kinkel LL (2009) Resource amendments influence density and competitive phenotypes of Streptomyces in soil. Microb Ecol 57(3):413–420. https://doi.org/10.1007/s00248-008-9433-4

    Article  PubMed  Google Scholar 

  68. Kinkel LL, Bakker MG, Schlatter DC (2011) A coevolutionary framework for managing disease-suppressive soils. Annu Rev Phytopathol 49:47–67. https://doi.org/10.1146/annurev-phyto-072910-095232

    Article  CAS  PubMed  Google Scholar 

  69. 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 409(1-2):329–343. https://doi.org/10.1007/s11104-016-2968-0

    Article  CAS  Google Scholar 

  70. Wiggins BE, Kinkel LL (2005a) Green manures and crop sequences influence potato diseases and pathogen inhibitory activity of indigenous streptomycetes. Phytopathol 95:178–185. https://doi.org/10.1094/PHYTO-95-0178

    Article  CAS  Google Scholar 

  71. Wiggins BE, Kinkel LL (2005b) Green manures and crop sequences influence alfalfa root rot and pathogen inhibitory activity among soil-borne streptomycetes. Plant Soil 268(1-2):271–283. https://doi.org/10.1007/s11104-004-0300-x

    Article  CAS  Google Scholar 

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

    Google Scholar 

  73. Baines ALD, Xiao K, Kinkel LL (2007) Lack of correspondence between genetic and phenotypic groups amongst soil-borne streptomycetes. FEMS Microbiol Ecol 59:564–575. https://doi.org/10.1111/j.1574-6941.2006.00231

    Article  CAS  Google Scholar 

  74. Lorang JM, Liu D, Anderson NA, Schottel JL (1995) Identification of potato scab inducing and suppressive species of Streptomyces. Phytopathol 85:261–268. https://doi.org/10.1094/Phyto-85-261

    Article  Google Scholar 

  75. SAS 9.2, SAS Institute Inc., Cary, N. C., USA.

  76. GraphPad Prism 5.03, GraphPad Software Inc., La Jolla, C. A., USA

  77. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

  78. Bakker MG, Schlatter DC, Otto-Hanson LK, Kinkel LL (2014) Diffuse symbioses: role of plant-plant, plant-microbe, and microbe-microbe interactions in structuring the soil microbiome. Mol Ecol 23(6):1571–1583. https://doi.org/10.1111/mec.12571

    Article  PubMed  Google Scholar 

  79. Seuradge BJ, Oelbermann M, Neufeld JD (2017) Depth-dependent influence of different land-use systems on bacterial biogeography. FEMS Microbiol Ecol 93(2):1–17. https://doi.org/10.1093/femsec/fiw239

    Article  CAS  Google Scholar 

  80. Zhang Q, Goberna M, Liu YG, Cui M, Yang HS, Sun QX, Insam H, Zhou JX (2018) Competition and habitat filtering jointly explain phylogenetic structure of soil bacterial communities across elevational gradients. Environ Microbiol 20(8):2386–2396. https://doi.org/10.111/1462-2920.14247

  81. Czárán TL (2002) Chemical warfare between microbes promotes biodiversity. Proc Natl Acad Sci U S A 99:786–790

    Article  Google Scholar 

  82. Akhter N, Liu Y, Auckloo BN, Shi Y, Wang K, Chen J, Wu X, Wu B (2018) Stress-driven discovery of new angucycline-type antibiotics from a marine Streptomyces pratensis NA-ZhouS1. Mar Drugs 16:331

    Article  Google Scholar 

  83. Rodrigues KCS, Costa CLL, Badino AC, Pedrolli DB, Pereira JFB, Cerri MO (2019) Application of acid and cold stress to enhance production of clavulanic acid by Streptomyces clavuligerus. Appl Biochem Biotechnol 188:706–719

    Article  CAS  Google Scholar 

  84. Brady NC (1990) Organisms of the soil. In the Nature and Property of Soils, 10th edn, (pp. 253-277) Macmillan Publishing Company, New York, New York.

  85. Kontro M, Lignell U, Hirvonen MR, Nevalainen A (2005) pH effects on 10 Streptomyces spp. growth and sporulation depend on nutrients. Lett Appl Microbiol 41(1):32–38

    Article  CAS  Google Scholar 

  86. Wolf AB, Vos M, deBoer W, Kowalchuk GA (2013) Impact of matric potential and pore size distribution on growth dynamics of filamentous and non-filamentous soil bacteria. PLoS One 8(12):e83661. https://doi.org/10.1371/journal.pone.0083661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank Maia Dedrick for performing the modified Herr’s assay on the soil samples. We fully appreciate the rigorous sampling efforts of the members of the Kinkel Lab: Maia Dedrick, Jon Anderson, Patricia Vaz-Jauri, Atenea Garza, Matt Bakker, Dan Schlatter, and A.J. Lange. We also gratefully acknowledge the contributions of Seth Spawn and Sarah Castle to the statistical analyses.

Funding

Finally, we appreciate the support of the National Science Foundation Microbial Observatories Project 9977907 and the United States Department of Agriculture Microbial Observatories Program Grant 2006-35319-17445 in funding the research project.

Author information

Authors and Affiliations

  1. University of Minnesota-Twin Cities, 1991 Upper Buford Circle, 495 Borlaug Hall, Saint Paul, MN, 55108, USA

    L. K. Otto-Hanson & L. L. Kinkel

Authors
  1. L. K. Otto-Hanson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. L. Kinkel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. K. Otto-Hanson.

Electronic supplementary material

ESM 1

(DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Otto-Hanson, L.K., Kinkel, L.L. Densities and inhibitory phenotypes among indigenous Streptomyces spp. vary across native and agricultural habitats. Microb Ecol 79, 694–705 (2020). https://doi.org/10.1007/s00248-019-01443-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-019-01443-2

Keywords

Search

Navigation