Abstract

Multicellular cooperation in actinomycetes is a division of labor-based beneficial trait where phenotypically specialized clonal subpopulations, or genetically distinct lineages, perform complementary tasks. The division of labor improves the access to nutrients and optimizes reproductive and vegetative tasks while reducing the costly production of secondary metabolites and/or of secreted enzymes. In this study, we took advantage of the possibility to isolate genetically distinct lineages deriving from the division of labor, for the isolation of heterogeneous teicoplanin producer phenotypes from Actinoplanes teichomyceticus ATCC 31121. In order to efficiently separate phenotypes and associated genomes, we produced and regenerated protoplasts. This approach turned out to be a rapid and effective strain improvement method, as it allowed the identification of those phenotypes in the population that produced higher teicoplanin amounts. Interestingly, a heterogeneous teicoplanin complex productivity pattern was also identified among the clones. This study suggests that strain improvement and strain maintenance should be integrated with the use of protoplasts as a strategy to unravel the hidden industrial potential of vegetative mycelium.

Highlights

  • Division of labor is a common feature in natural systems and can be found at different levels of biological organization, from the individuals in a shared society to the cells of a single multicellular organism

  • This study suggests that strain improvement and strain maintenance should be integrated with the use of protoplasts as a strategy to unravel the hidden industrial potential of vegetative mycelium

  • The possibility to separate genomes within the complex population of A. teichomyceticus can be of paramount importance for industrial purposes, to select only those members of the population actively devoted to teicoplanin production

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Summary

Introduction

Division of labor is a common feature in natural systems and can be found at different levels of biological organization, from the individuals in a shared society to the cells of a single multicellular organism. Examples of division of labor among colony subpopulations that specialize to perform different cooperative tasks have been extensively described [1,2]. Filamentous actinomycetes are microorganisms that grow to form complex structures in which the alternation of vegetative and reproductive growth phases represents an example of division of labor. In the model actinomycete Streptomyces coelicolor, it was reported that metabolically costly antibiotic production and secretion represents a trade-off with growth, and is performed by only a fraction of the hyphae, which could eventually lose the possibility to produce spores and to propagate, identified as the “sterile caste” [7,8]. As the sterile caste displays a maximization in the diversity and production of secreted antibiotics [7], the capacity to identify and preserve it in an industrial setting may represent an opportunity for selecting industrially relevant lineages (i.e., high producers or producers of new antibiotics) [8]

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