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A squalene–hopene cyclase in *Schizosaccharomyces japonicus *represents a eukaryotic adaptation to sterol–independent anaerobic growth


Biosynthesis of sterols, which are key constituents of canonical eukaryotic membranes, requires molecular oxygen. Anaerobic protists and deep-branching anaerobic fungi are the only eukaryotes in which a mechanism for sterol-independent growth has been elucidated. In these organisms, tetrahymanol, formed through oxygen-independent cyclization of squalene by a squalene-tetrahymanol cyclase, acts as a sterol surrogate. This study confirms an early report (Bulder (1971), Antonie Van Leeuwenhoek, 37, 353–358) that Schizosaccharomyces japonicus is exceptional among yeasts in growing anaerobically on synthetic media lacking sterols and unsaturated fatty acids.

Mass spectrometry of lipid fractions of anaerobically grown Sch. japonicus showed the presence of hopanoids, a class of cyclic triterpenoids not previously detected in yeasts, including hop-22(29)-ene, hop-17(21)-ene, hop-21(22)-ene and hopan-22-ol. A putative gene in Sch. japonicus showed high similarity to bacterial squalene-hopene cyclase (SHC) genes and in particular to those of Acetobacter species. No orthologs of the putative Sch. japonicus SHC were found in other yeast species.

Expression of the Sch. japonicus SHC gene (Sjshc1) in Saccharomyces cerevisiae enabled hopanoid synthesis and supported ergosterol-independent anaerobic growth, thus confirming that one or more of the hopanoids produced by SjShc1 can act as ergosterol surrogate in anaerobic yeast cultures. Use of hopanoids as sterol surrogates represents a previously unknown adaptation of eukaryotic cells to anaerobic growth. The fast sterol-independent anaerobic growth of Sch. japonicus is an interesting trait for developing robust fungal cell factories for application in anaerobic industrial processes.

Authors: Jonna Bouwknegt, Sanne J. Wiersma, Raúl A. Ortiz-Merino, Eline S. R. Doornenbal, Petrik Buitenhuis, Martin Giera, Christoph Müller, Jack T. Pronk

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