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. 2019 Jul 2;10(1):2916.
doi: 10.1038/s41467-019-10983-7.

Essentiality of Sterol Synthesis Genes in the Planctomycete Bacterium Gemmata Obscuriglobus

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Free PMC article

Essentiality of Sterol Synthesis Genes in the Planctomycete Bacterium Gemmata Obscuriglobus

Elena Rivas-Marin et al. Nat Commun. .
Free PMC article

Abstract

Sterols and hopanoids are chemically and structurally related lipids mostly found in eukaryotic and bacterial cell membranes. Few bacterial species have been reported to produce sterols and this anomaly had originally been ascribed to lateral gene transfer (LGT) from eukaryotes. In addition, the functions of sterols in these bacteria are unknown and the functional overlap between sterols and hopanoids is still unclear. Gemmata obscuriglobus is a bacterium from the Planctomycetes phylum that synthesizes sterols, in contrast to its hopanoid-producing relatives. Here we show that sterols are essential for growth of G. obscuriglobus, and that sterol depletion leads to aberrant membrane structures and defects in budding cell division. This report of sterol essentiality in a prokaryotic species advances our understanding of sterol distribution and function, and provides a foundation to pursue fundamental questions in evolutionary cell biology.

Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1
Terbinafine treatment suppresses growth and sterol production in Gemmata obscuriglobus, in a concentration-dependent manner. a Terbinafine (TB) treatment at various concentrations inhibits G. obscuriglobus growth relative to untreated cultures, measured spectrophotometrically over a 6-day time-course. Means and standard deviations are shown for three biological replicates. The points are represented by circles, upside-down triangles, triangles, and diamonds for increasing terbinafine concentrations, respectively. b Total cellular sterols, measured using gas chromatography-mass spectrometry at 3-day and 6-day culture growth time points. Data is presented in boxplot of four biological replicates, each analyzed in triplicate. The center line represents the median, the box represents the upper and lower quartiles, and the lines represent the minimum and maximum observations. Any points outside the lines are considered outliers. c Lanosterol supplementation of TB-treated cultures partially or completely restores growth to the level of untreated cultures, measured spectrophotometrically at 3-day and 6-day culture growth time points. Means and standard deviations are shown for three biological replicates. Source data are provided as a Source Data file
Fig. 2
Fig. 2
Transmission electron microscopy of G. obscuriglobus cells deficient in sterol synthesis. Representative membrane phenotypes observed in the G. obscuriglobus mutant interrupted in the sqmo gene. Wild-type cell (a). Various membrane organizations are shown, including b cellular space crowded with small vesicles, c stacks of membrane layers inside the cytoplasm, d multiple elongated sausage-like structures, e, f or a mixture of these and undefined features, g multiple budding. g, h Arrows indicate necks between dividing cells. Black dots correspond to localization of the GFP used to interrupt the sqmo gene. Scale bar represents 0.5 μm
Fig. 3
Fig. 3
Terbinafine treatment inhibits normal budding replication in Gemmata obscuriglobus. Selected frames of phase-contrast time-lapse microscopy of 4-day G. obscuriglobus cultures. a Control culture. b Culture treated with 100 μg mL−1 terbinafine. c Culture treated with 100 μg mL−1 terbinafine and 1 μg mL−1 lanosterol. ac Scale bar represents 1 μm. d Incidence of phase-bright inclusions in TB-treated culture with or without lanosterol supplementation. Phase-bright inclusions were never observed in untreated cultures. Means and standard deviations are shown for three biological replicates. Source data are provided as a Source Data file

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