Lipid metabolism dysfunction following symbiont elimination is linked to altered Kennedy pathway homeostasis

Geoffrey M Attardo; Joshua B Benoit; Veronika Michalkova; Alekhya Kondragunta; Aaron A Baumann; Brian L Weiss; Anna Malacrida; Francesca Scolari; Serap Aksoy

doi:10.1016/j.isci.2023.107108

Lipid metabolism dysfunction following symbiont elimination is linked to altered Kennedy pathway homeostasis

iScience. 2023 Jun 12;26(7):107108. doi: 10.1016/j.isci.2023.107108. eCollection 2023 Jul 21.

Authors

Geoffrey M Attardo^{1

2}, Joshua B Benoit^{1

3}, Veronika Michalkova^{1

4}, Alekhya Kondragunta³, Aaron A Baumann^{1

5}, Brian L Weiss¹, Anna Malacrida⁶, Francesca Scolari^{6

7}, Serap Aksoy¹

Affiliations

¹ Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, USA.
² Department of Entomology and Nematology, Division of Agriculture and Natural Resources, University of California Davis, Davis, CA 95616, USA.
³ Department of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221, USA.
⁴ Section of Molecular and Applied Zoology, Institute of Zoology, Slovak Academy of Sciences, Bratislava, Slovakia.
⁵ Center for Agricultural Synthetic Biology, University of Tennessee, Knoxville, TN 37996, USA.
⁶ Department of Biology and Biotechnology, University of Pavia, 27100 Pavia, Italy.
⁷ Institute of Molecular Genetics (IGM), Italian National Research Council (CNR), Via Abbiategrasso 207, 27100 Pavia, Italy.

Abstract

Lipid metabolism is critical for insect reproduction, especially for species that invest heavily in the early developmental stages of their offspring. The role of symbiotic bacteria during this process is understudied but likely essential. We examined the role of lipid metabolism during the interaction between the viviparous tsetse fly (Glossina morsitans morsitans) and its obligate endosymbiotic bacteria (Wigglesworthia glossinidia) during tsetse pregnancy. We observed increased CTP:phosphocholine cytidylyltransferase (cct1) expression during pregnancy, which is critical for phosphatidylcholine biosynthesis in the Kennedy pathway. Experimental removal of Wigglesworthia impaired lipid metabolism via disruption of the Kennedy pathway, yielding obese mothers whose developing progeny starve. Functional validation via experimental cct1 suppression revealed a phenotype similar to females lacking obligate Wigglesworthia symbionts. These results indicate that, in Glossina, symbiont-derived factors, likely B vitamins, are critical for the proper function of both lipid biosynthesis and lipolysis to maintain tsetse fly fecundity.

Keywords: Bacteriology; Physiology.

Abstract

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