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Widespread predatory abilities in the genus Streptomyces

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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.

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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.

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Authors and Affiliations

  1. Anujeeva Biosciences Pvt Ltd, Pune, 411038, Maharashtra, India

    Charushila Kumbhar & Milind Watve

  2. Department of Microbiology, Abasaheb Garware College, Karve Road, Pune, 411004, Maharashtra, India

    Charushila Kumbhar & Praneitha Mudliar

  3. Indian Institute of Science Education and Research (IISER), First floor, Central Tower, Sai Trinity Building Garware Circle, Sutarwadi, Pashan, Pune, 411021, Maharashtra, India

    Charushila Kumbhar, Latika Bhatia, Aseem Kshirsagar & Milind Watve

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  1. Charushila Kumbhar
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  4. Aseem Kshirsagar
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Correspondence to Milind Watve.

Additional information

Communicated by Erko Stackebrandt.

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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)

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

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