Advertisement

Archives of Microbiology

, Volume 196, Issue 4, pp 235–248 | Cite as

Widespread predatory abilities in the genus Streptomyces

  • Charushila Kumbhar
  • Praneitha Mudliar
  • Latika Bhatia
  • Aseem Kshirsagar
  • Milind WatveEmail author
Original Paper

Abstract

The natural role of antibiotics in the ecology of Streptomyces is debated and still largely unknown. The predatory myxobacteria and many other genera of prokaryotic epibiotic and wolfpack predators across different taxa possess secondary metabolites with antimicrobial action, and these compounds have a role in predation. If all epibiotic predators are antibiotic producers, it is worth testing whether all antibiotic producers are predators too. We show here that Streptomyces are non-obligate epibiotic predators of other microorganisms and that predatory abilities are widespread in this genus. We developed a test for predatory activity which revealed that a large proportion of traditionally isolated Streptomyces strains and all oligophilic Streptomyces isolates show predatory activity. Those that did not show predatory ability on first challenge could do so after many generations of selection or acclimation. Using time-lapse photomicrography, we demonstrate that the growth of the tips of Streptomyces hyphae is accompanied by disappearance of cells of other bacteria in the vicinity presumably due to lysis. Predatory activity is restricted to surface growth and is not obligately associated with antibiotic production in conventional culture. However, some of the genes crucial to the regulation of secondary metabolite pathways are differentially expressed during predatory growth on different prey species as compared to saprophytic growth. Our findings strengthen the association between epibiotic predation and antibiotic production.

Keywords

Predation Antibiotic production Streptomyces Secondary metabolite 

Notes

Acknowledgments

We gratefully acknowledge the material, technical, and intellectual contributions of Anjan Banerjee, Neelesh Dahanukar, Geeta Khaladkar, and Anagha Kale. We thank David Hopwood and Mervyn Bibb (John Innes Center) for the strain Streptomyces coelicolor A3(2) and Deepa Kanitkar of KanBiosys for the availability of some of the prey species. Earlier phase of the work was financed by LABINDIA.

Supplementary material

203_2014_961_MOESM1_ESM.pdf (5.1 mb)
Supplementary material 1 (PDF 5248 kb)

Supplementary material 2 Growth of mycelial tips (advancing from the top downwards) accompanied by disappearance of prey cells (bottom half). The movie is created from time-lapse photomicrography at an interval of 10 minutes. (WMV 6521 kb)

Supplementary material 3 Growth of mycelial tips through uneven prey cell distribution, large clusters interspersed by scattered cells. Note that cell disappearance is faster in low cell density areas. The movie is created from time-lapse photomicrography at an interval of 10 minutes. (WMV 4923 kb)

Supplementary material 4 Difference in cell appearance and cell density away from and close to predator growth. The movie is a pan going from the center of the predator colony over the edge and away from it. Prey cell density was even before predator inoculation. After predator growth, no prey cells are visible within the predator colony, at the edge where growing mycelial tips can be seen a large proportion of prey cells are seen as dark flat disintegrated cells and farther away from the colony intact elevated appearance of prey cells is evident. (MPG 2206 kb)

References

  1. Abramoff M, Magelhaes P, Ram S (2004) Image processing with image. J Biophoto Int 11:36–42Google Scholar
  2. Adamidis T, Riggle P, Champness W (1990) Mutations in a new Streptomyces coelicolor locus which globally block antibiotic biosynthesis but not sporulation. J Bacteriol 172:2962–2969PubMedCentralPubMedGoogle Scholar
  3. Adegboye M, Babalola O (2012) Taxonomy and ecology of antibiotic producing actinomycetes. Afr J Agri Res 7:2255–2261Google Scholar
  4. Baba T, Schneewind O (1998) Instruments of microbial warfare: bacteriocin synthesis, toxicity and immunity. Trends Microbiol 6:66–71PubMedCrossRefGoogle Scholar
  5. Baltz R (2007) Antimicrobials from actinomycetes: back to the future. Microbe Mag 2:125–131Google Scholar
  6. Banerjee A, Lin T, Hannapel D (2009) Ultratranslated regions of a mobile transcript mediate RNA metabolism. Plant Physiol 151:1831–1843PubMedCentralPubMedCrossRefGoogle Scholar
  7. Bentley S, Chater K, Cerdeno-Tarraga A, Challis G, Thomson N et al (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147PubMedCrossRefGoogle Scholar
  8. Berleman J, Scott J, Chumley T, Kirby J (2008) Predataxis behavior in Myxococcus xanthus. Proc Natl Acad Sci USA 105:17127–17132PubMedCentralPubMedCrossRefGoogle Scholar
  9. Casida L (1980) Bacterial predators of Micrococcus luteus in soil. Appl Environ Microbiol 39:1035–1041PubMedCentralPubMedGoogle Scholar
  10. Casida L (1982) Ensifer adhaerens Gen. Nov., Sp. Nov.: a bacterial predator of bacteria in soil†. Int J Syst Bacteriol 32:339–345CrossRefGoogle Scholar
  11. Casida L (1983) Interaction of Agromyces ramosus with other bacteria in soil. Appl Environ Microbiol 46:881–888PubMedCentralPubMedGoogle Scholar
  12. Casida L (1988) Minireview: nonobligate bacterial predation of bacteria in soil. Microbial Ecol 15:1–8CrossRefGoogle Scholar
  13. Challis G, Hopwood D (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci USA 100(Suppl 2):14555–14561PubMedCentralPubMedCrossRefGoogle Scholar
  14. Chater K, Biro S, Lee K, Palmer T, Schrempd H (2010) The complex extracellular biology of Streptomyces. FEMS Microbiol Rev 34:171–198PubMedCrossRefGoogle Scholar
  15. Currie C (2001) A community of ants, fungi, and bacteria: a multilateral approach to studying symbiosis. Annu Rev Microbiol 55:357–380PubMedCrossRefGoogle Scholar
  16. Currie C, Bot A, Boomsma J (2003a) Experimental evidence of a tripartite mutualism: bacteria protect ant fungus gardens from specialized parasites. Oikos 101:91–102CrossRefGoogle Scholar
  17. Currie C, Scott J, Summerbell R, Malloch D (2003b) Corrigendum: fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 423:461CrossRefGoogle Scholar
  18. Currie C, Poulsen M, Mendenhall J, Boomsma J, Billen J (2006) Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science 311:81–83PubMedCrossRefGoogle Scholar
  19. Dworkin M, Rosenberg E, Schleifer K (2006) The prokaryotes: ecophysiology and biochemistry, vol 2, 3rd edn. Springer Press, SingaporeCrossRefGoogle Scholar
  20. Fredrickson A, Stephanopoulos G (1981) Microbial competition. Science 213:972–979PubMedCrossRefGoogle Scholar
  21. Germida J, Casida L (1983) Ensifer adhaerens predatory activity against other bacteria in soil, as monitored by indirect phage analysis. Appl Environ Microbiol 45:1380–1388PubMedCentralPubMedGoogle Scholar
  22. Goodfellow M, Williams S (1983) Ecology of actinomycetes. Annu Rev Microbiol 37:189–216PubMedCrossRefGoogle Scholar
  23. Gottlieb D (1976) The production and role of antibiotics in soil. J Antibiot 29:987–1000PubMedCrossRefGoogle Scholar
  24. Hartmann T (2007) From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochemistry 68:2831–2846PubMedCrossRefGoogle Scholar
  25. Haslam E (1986) Secondary metabolism—fact and fiction. Nat Prod Rep 3:217–249CrossRefGoogle Scholar
  26. Hillesland K, Velicer G, Lenski R (2009) Experimental evolution of a microbial predator’s ability to find prey. Proc Biol Sci 276:459–467PubMedCentralPubMedCrossRefGoogle Scholar
  27. Jayapal K, Lian W, Glod F, Sherman D, Hu W (2007) Comparative genomic hybridizations reveal absence of large Streptomyces coelicolor genomic islands in Streptomyces lividans. BMC Genomics 8:229PubMedCentralPubMedCrossRefGoogle Scholar
  28. Jenke-Kodama H, Müller R, Dittmann E (2008) Evolutionary mechanisms underlying secondary metabolite diversity. Prog Drug Res 65(119):121–140Google Scholar
  29. Kaltenpoth M, Göttler W, Herzner G, Strohm E (2005) Symbiotic bacteria protect wasp larvae from fungal infestation. Curr Biol 15:475–479PubMedCrossRefGoogle Scholar
  30. Katz E, Demain A (1977) The peptide antibiotics of Bacillus: chemistry, biogenesis, and possible functions. Bacteriol Rev 41:449–474PubMedCentralPubMedGoogle Scholar
  31. Kolter R, Moreno F (1992) Genetics of ribosomally synthesized peptide antibiotics. Annu Rev Microbiol 46:141–161PubMedCrossRefGoogle Scholar
  32. Kroiss J, Kaltenpoth M, Schneider B, Schwinger M, Hertweck C et al (2010) Symbiotic streptomycetes provide antibiotic combination prophylaxis for wasp offspring. Nat Chem Biol 6:261–263PubMedCrossRefGoogle Scholar
  33. Kumbhar C, Watve M (2013) Why antibiotics: a comparative evaluation of different hypotheses for the natural role of antibiotics and an evolutionary synthesis. Nat Sci 5:26–40Google Scholar
  34. Linares J, Gustafsson I, Baquero F, Martinez J (2006) Antibiotics as intermicrobial signaling agents instead of weapons. Proc Natl Acad Sci USA 103:19484–19489PubMedCentralPubMedCrossRefGoogle Scholar
  35. Luckner M (1972) Secondary metabolism in plants and animals, 2nd edn. Springer, BerlinGoogle Scholar
  36. Malik V (1980) Microbial secondary metabolism. Trends Biochem Sci 5:68–72CrossRefGoogle Scholar
  37. Martin J, Demain A (1980) Control of antibiotic biosynthesis. Microbiol Rev 44:230–251PubMedCentralPubMedGoogle Scholar
  38. Mothes K (1955) Physiology of alkaloids. Annu Rev Plant Physiol 6:393–432CrossRefGoogle Scholar
  39. Nett M, Ikeda H, Moore B (2009) Genomic basis for natural product biosynthetic diversity in the actinomycetes. Nat Prod Rep 26:1362–1384PubMedCentralPubMedCrossRefGoogle Scholar
  40. Nützmanna H, Reyes-Dominguez Y, Scherlach K, Schroeckh V, Horn F et al (2011) Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation. Proc Natl Acad Sci USA 108:14282–14287CrossRefGoogle Scholar
  41. Pérez J, Muñoz-Dorado J, Braña A, Shimkets L, Sevillano L, Santamaría R (2011) Myxococcus xanthus induces actinorhodin overproduction and aerial mycelium formation by Streptomyces coelicolor. Microbial Biotechnol 4:175–183CrossRefGoogle Scholar
  42. Robinson T (1974) Metabolism and function of alkaloids in plants. Science 184:430–435PubMedCrossRefGoogle Scholar
  43. Rosamond J, Allsop A (2000) Harnessing the power of the genome in the search for new antibiotics. Science 287:1973–1976PubMedCrossRefGoogle Scholar
  44. Schroeckh V, Scherlach K, Nützmanna H, Shelest E, Schmidt-Heck W et al (2009) Intimate bacterial–fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci 106:14558–14563PubMedCentralPubMedCrossRefGoogle Scholar
  45. Seigler D (1998) Plant secondary metabolism. Kluwer Academic publisher, Massachusetts, p 759CrossRefGoogle Scholar
  46. Straight P, Willey J, Kolter R (2006) Interactions between Streptomyces coelicolor and Bacillus subtilis: role of surfactants in raising aerial structures. J Bacteriol 188:4918–4925PubMedCentralPubMedCrossRefGoogle Scholar
  47. Swain T (1977) Secondary compounds as protective agents. Annu Rev Plant Physiol 28:479–501CrossRefGoogle Scholar
  48. Turner W (1971) Fungal metabolites. Academic press, London, p 446Google Scholar
  49. Udwary D, Zeigler L, Asolkar R, Singan V, Lapidus A et al (2007) Genome sequencing reveals complex secondary metabolome in the marine actinomycete Salinispora tropica. Proc Natl Acad Sci USA 104:10376–10381PubMedCentralPubMedCrossRefGoogle Scholar
  50. Ueda K, Kawai S, Ogawa H, Kiyama A, Kubota T (2000) Wide distribution of interspecific stimulatory events on antibiotic production and sporulation among Streptomyces species. J Antibiot 53:979–982PubMedCrossRefGoogle Scholar
  51. Vining L (1990) Functions of secondary metabolites. Annu Rev Microbiol 44:395–427PubMedCrossRefGoogle Scholar
  52. Waksman S, Woodruff H (1941) Actinomyces antibioticus, a new soil organism antagonistic to pathogenic and non-pathogenic bacteria. J Bacteriol 42:231–249PubMedCentralPubMedGoogle Scholar
  53. Watve M, Kumbhar C (2007) Streptomyces sp. as predators of bacteria. Nat Preced. doi: 10.1038/npre.2007.1263.2
  54. Watve M, Shejval V, Sonawane C, Rahalkar M, Matapurkar A et al (2000) The “K” selected oligophilic bacteria: a key to uncultured diversity? Curr Sci 78:1535–1542Google Scholar
  55. Watve M, Tickoo R, Jog M, Bhole B (2001) How many antibiotics are produced by the genus Streptomyces? Arch Microbiol 176:386–390PubMedCrossRefGoogle Scholar
  56. Welsch M (1962) Bacteriolytic enzymes from streptomycetes: a review. J Gen Physiol 45:115–124PubMedCentralPubMedCrossRefGoogle Scholar
  57. Williams S, Vickers J (1986) The ecology of antibiotic production. Microb Ecol 12:43–52PubMedCrossRefGoogle Scholar
  58. Williams D, Stone M, Hauck P, Rahman S (1989) Why are secondary metabolites (natural products) biosynthesized? J Nat Prod 52:1189–1208PubMedCrossRefGoogle Scholar
  59. Wu G, Culley D, Zhang W (2005) Predicted highly expressed genes in the genomes of Streptomyces coelicolor and Streptomyces avermitilis and the implications for their metabolism. Microbiology 151:2175–2187PubMedCrossRefGoogle Scholar
  60. Xiao Y, Wei X, Ebright R, Wall D (2011) Antibiotic production by myxobacteria plays a role in predation. J Bacteriol 193:4626–4633PubMedCentralPubMedCrossRefGoogle Scholar
  61. Yamamoto Y, Kouchiwa T, Hodoki Y, Hotta K, Uchida H, Harada K (1998) Distribution and identification of actinomycetes lysing cyanobacteria in a eutrophic lake. J Appl Phycol 10:391–397CrossRefGoogle Scholar
  62. Zeph L, Casida L (1986) Gram-negative versus gram-positive (actinomycete) nonobligate bacterial predators of bacteria in soil. Appl Environ Microbiol 52:819–823PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Charushila Kumbhar
    • 1
    • 2
    • 3
  • Praneitha Mudliar
    • 2
  • Latika Bhatia
    • 3
  • Aseem Kshirsagar
    • 3
  • Milind Watve
    • 1
    • 3
    Email author
  1. 1.Anujeeva Biosciences Pvt LtdPuneIndia
  2. 2.Department of MicrobiologyAbasaheb Garware CollegePuneIndia
  3. 3.Indian Institute of Science Education and Research (IISER)PuneIndia

Personalised recommendations