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. 2021 Jan 29;24(2):102115.
doi: 10.1016/j.isci.2021.102115. eCollection 2021 Feb 19.

Shotgun lipidomics and mass spectrometry imaging unveil diversity and dynamics in Gammarus fossarum lipid composition

Tingting Fu  1 , Oskar Knittelfelder  2 , Olivier Geffard  3 , Yohann Clément  1 , Eric Testet  4 , Nicolas Elie  5 , David Touboul  5 , Khedidja Abbaci  3 , Andrej Shevchenko  2 , Jerome Lemoine  1 , Arnaud Chaumot  3 , Arnaud Salvador  1 , Davide Degli-Esposti  3 , Sophie Ayciriex  1
Affiliations

Shotgun lipidomics and mass spectrometry imaging unveil diversity and dynamics in Gammarus fossarum lipid composition

Tingting Fu et al. iScience. .

Abstract

Sentinel species are playing an indispensable role in monitoring environmental pollution in aquatic ecosystems. Many pollutants found in water prove to be endocrine disrupting chemicals that could cause disruptions in lipid homeostasis in aquatic species. A comprehensive profiling of the lipidome of these species is thus an essential step toward understanding the mechanism of toxicity induced by pollutants. Both the composition and spatial distribution of lipids in freshwater crustacean Gammarus fossarum were extensively examined herein. The baseline lipidome of gammarids of different sex and reproductive stages was established by high throughput shotgun lipidomics. Spatial lipid mapping by high resolution mass spectrometry imaging led to the discovery of sulfate-based lipids in hepatopancreas and their accumulation in mature oocytes. A diverse and dynamic lipid composition in G. fossarum was uncovered, which deepens our understanding of the biochemical changes during development and which could serve as a reference for future ecotoxicological studies.

Keywords: Environmental Science; Lipidomics; Metabolomics; Pollution; Zoology.

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Conflict of interest statement

The authors declare no competing interests.

Figures

None
Graphical abstract
Figure 1
Figure 1
Lipid composition of the Gammarus fossarum lipidome (A) Lipid classes identified in G. fossarum organism with the associated number of lipid species identified. Comparison of the different lipid profile between male and female gammarids at specific female reproductive stages (C1 versus D1). (B) TAG profile. (C) Cholesterol, phosphatidylcholine, phosphatidylethanolamine, and ether lipid distribution. (D) Lysophospholipid, phosphatidylinositol, and sphingomyelin profile. Lipid class abundance is presented as moles per mole of total membrane lipid (phospholipids, sphingolipids, and sterols – not including storage lipids). Significance was calculated by Student's t test, and statistically significant changes (∗∗∗p < 0.001) are marked by asterisks. Data are represented as mean +/− standard deviation.
Figure 2
Figure 2
Diverse molecular lipid species in G. fossarum across gender and female reproductive stages Lipid profile for the main glycerolipid (A) TAG and the two main phospholipid classes (B) PC and (C) PE. (D) Sphingomyelin profile. Note that for TAG profile only the species higher than 5 mol% are presented. Significance was calculated by Student's t test, and statistically significant changes (∗∗p < 0.01, ∗∗∗p < 0.001) are marked by asterisks. Data are represented as mean +/− standard deviation.
Figure 3
Figure 3
Localization of lipids in whole-body gammarid section by MALDI MSI (A) Optical image of the whole-body tissue section of the male gammarid. Scale bar, 2mm. (B) Ion image of protonated PC 34:1. (C) Ion image of sodium adduct of PC 34:1. (D) Ion image of potassium adduct of PC 34:1. (E) Ion image of potassium adduct of PC 36:3. (F) Ion image of the ion at m/z 841.5. (G) Two-color overlay of the ion at m/z 841.5 and the potassium adduct of PC 34:1. (I) Overlay of the two-color overlay image in G and the optical image. Ce: cephalon; ADS: anterior digestive system; HP: hepatopancreas; TS: thorax segments.
Figure 4
Figure 4
Lipid distribution in targeted organs of male gammarid by high-resolution SIMS imaging (A) Optical image of the gammarid tissue section. Scale bar, 2mm. (B) Ion images of lipid species detected in positive ion mode in ROI 1. (C) Ion images of lipid species detected in negative ion mode in ROI (D) Ion images of lipid species detected in positive ion mode in ROI 2. (E) Ion images of lipid species detected in negative ion mode in ROI 2. Ion image of vitamin E was summed from those of ions at m/z 429.4 (C29H49O2+ [M + H-2H]+) and m/z 430.4 (C29H49O2+· M+·). Ion image of m/z 634.4–696.4 was summed from those of ions at m/z 634.4, 648.5, 648.4, 664.5, 666.4, 680.4, 682.4, and 696.4. Ion image of m/z 588.5–618.5 was summed from those of ions at m/z 588.5, 602.5, 604.5, 616.5, and 618.5. ROI: region of interest; H: hemocoel; HP: hepatopancreas; G. gonad; M: muscle.
Figure 5
Figure 5
Identification of sulfate-based lipid species in the hepatopancreas (A) Ion images of selected chemical species detected in positive ion mode. Scale bar, 500 μm. (B) Ion images of selected chemical species detected in negative ion mode. (C) MS/MS spectrum of the precursor ion at m/z 588.4667 acquired on a QExactive mass spectrometer in negative ion mode. HP: hepatopancreas; M: muscle; IN: intestine.
Figure 6
Figure 6
Dynamic change in oocyte lipid composition during the reproductive cycle (A) Optical image of the transvers tissue section of C1 female and ion images of FA18:1 and sulfate-based lipids. Scale bar, 500 μm. (B) Optical image of the transvers tissue section of D1 female and ion images of FA 18:1 and sulfate-based lipids. Scale bar, 500 μm. The ion image of sulfate-based lipids at m/z 588.5–618.5 was summed from those of m/z 588.5, m/z 602.5, m/z 604.5, m/z 616.5, and m/z 618.5.
See this image and copyright information in PMC

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