Abstract

The yeast Starmerella bombicola distinguishes itself from other yeasts by its potential of producing copious amounts of the secondary metabolites sophorolipids (SLs): these are glycolipid biosurfactants composed out of a(n) (acetylated) sophorose moiety and a lipid tail. Although SLs are the subject of numerous research papers and have been commercialized, e.g., in eco-friendly cleaning solutions, the natural function of SLs still remains elusive. This research article investigates several hypotheses for why S. bombicola invests that much energy in the production of SLs, and we conclude that the main natural function of SLs in S. bombicola is niche protection: (1) the extracellular storage of an energy-rich, yet metabolically less accessible carbon source that can be utilized by S. bombicola upon conditions of starvation with (2) antimicrobial properties. In this way, S. bombicola creates a dual advantage in competition with other microorganisms. Additionally, SLs can expedite growth on rapeseed oil, composed of triacylglycerols which are hydrophobic substrates present in the yeasts’ environment, for a non-SL producing strain (Δcyp52M1). It was also found that—at least under lab conditions—SLs do not provide protection against high osmotic pressure prevalent in sugar-rich environments such as honey or nectar present in the natural habitat of S. bombicola.

Highlights

  • The name ‘Starmerella bombicola’ strongly associates with ‘biosurfactants’, as this species is the best known producer of sophorolipids, which are secondary metabolites: more than 75% of the research publications on this yeast focus on sophorolipids [1,2]

  • Precultures of E. coli, P. aeruginosa, and B. subtilis were grown on Lysogeny broth (10 g·L−1 tryptone, 5 g·L−1 yeast extract and 5 g·L−1 NaCl); H. alvei was cultivated on nutrient broth (Oxoid); S. aureus was cultivated on brain heart infusion broth (Biokar diagnostics); F. fructosus was cultivated on MRS broth (Thermo Fisher Scientific); C. albicans and S. bombicola were cultivated on 3C medium (100 g·L−1 glucose, 10 g·L−1 yeast extract, and 1 g·L−1 urea), and Z. rouxii was cultivated on YPD medium (5 g·L−1 yeast extract, 10 g·L−1 peptone and 20 g·L−1 glucose)

  • As already mentioned in the introduction, five hypotheses on the natural role of sophorolipids (SLs) for S. bombicola have been postulated. Four of those statements were investigated in this paper: (1) the antimicrobial activity of SLs, (2) the protection against high osmotic pressure, (3) an improved uptake of hydrophobic substrates, and (4) an extracellular storage compound

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Summary

Introduction

The name ‘Starmerella bombicola’ strongly associates with ‘biosurfactants’ (bio-based surface-active agents), as this species is the best known producer of sophorolipids, which are secondary metabolites: more than 75% of the research publications on this yeast focus on sophorolipids [1,2]. The SLs produced by S. bombicola are typically a mixture of several slightly different congeners providing each of them with specific properties [3,4,5,6,7,8]. SL molecules with a free carboxylic group are called acidic SLs and have good solubility in water. This carboxyl group can be esterified with the hydroxyl group on the C4” of sophorose forming a macrocyclic ring giving rise to lactonic SLs, which are characterized by low water solubility. Examples of other diversifications are: the length and saturation degree of the fatty acid chain (for S. bombicola, mainly C16:1 or C18:1), the position of attachment of the sophorose moiety (through a glycosidic bond) to the fatty acid at the ω (terminal) or ω-1 (sub-terminal) position, and the acetylation degree of sophorose (major structures are shown in Figure 1) [3,9,10]

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