Weevil endosymbiont dynamics is associated with a clamping of immunity.
BACKGROUND
Insects subsisting on nutritionally unbalanced diets have evolved long-term mutualistic relationships with intracellular symbiotic bacteria (endosymbionts). The endosymbiont population load undergoes changes along with insect development. In the cereal weevil Sitophilus oryzae, the midgut endosymbionts Sodalis pierantonius drastically multiply following adult metamorphosis and rapidly decline until total elimination when the insect achieves its cuticle synthesis. Whilst symbiont load was shown to timely meet insect metabolic needs, little is known about the host molecular and immune processes underlying this dynamics.


METHODS
We performed RNA sequencing analysis on weevil midguts at three representative phases of the endosymbiont dynamics (i.e. increase, climax and decrease). To screen genes which transcriptional changes are specifically related to symbiont dynamics and not to the intrinsic development of the midgut, we further have monitored by RT-qPCR sixteen gene transcript levels in symbiotic and artificially non-symbiotic (aposymbiotic) weevils. We also localized the endosymbionts during the elimination process by fluorescence microscopy.


RESULTS
Functional analysis of the host differentially expressed genes by RNA sequencing showed that the main transcriptional changes occur during endosymbiont growth phase and affect cell proliferation, apoptosis, autophagy, phagocytosis, and metabolism of fatty acids and nucleic acids. We also showed that symbiont dynamics alters the expression of several genes involved in insect development. Our results strengthened the implication of apoptosis and autophagy processes in symbiont elimination and recycling. Remarkably, apart from the coleoptericin A that is known to target endosymbionts and controls their division and location, no gene coding antimicrobial peptide was upregulated during the symbiont growth and elimination phases.


CONCLUSIONS
We show that endosymbiont dynamics parallels numerous transcriptional changes in weevil developing adults and affects several biological processes, including metabolism and development. It also triggers cell apoptosis, autophagy and gut epithelial cell swelling and delamination. Strikingly, immunity is repressed during the whole process, presumably avoiding tissue inflammation and allowing insects to optimize nutrient recovery from recycled endosymbiont.
Université de Lyon, INSA-Lyon, INRA, UMR203 BF2I, Biologie Fonctionnelle Insectes et Interactions, F-69621, Villeurbanne, France. florent.masson@insa-lyon.fr.
Florent
F
Masson
Université de Lyon, INSA-Lyon, INRA, UMR203 BF2I, Biologie Fonctionnelle Insectes et Interactions, F-69621, Villeurbanne, France. yves.mone@supagro.inra.fr.|Present address: Université Montpellier 2, INRA, UMR 1333 DGIMI, Diversité, Génomes et Interactions Micro-Organismes Insectes, F-34095, Montpellier, France. yves.mone@supagro.inra.fr.
Yves
Y
Moné
Université de Lyon, INSA-Lyon, INRA, UMR203 BF2I, Biologie Fonctionnelle Insectes et Interactions, F-69621, Villeurbanne, France. aurelien.vigneron@yale.edu.|Present address: Department of Epidemiology and Public Health, Division of Epidemiology of Microbial Diseases, Yale University School of Medicine, New Haven, CT, USA. aurelien.vigneron@yale.edu.
Aurélien
A
Vigneron
Université de Lyon, INSA-Lyon, INRA, UMR203 BF2I, Biologie Fonctionnelle Insectes et Interactions, F-69621, Villeurbanne, France. agnes.vallier@lyon.inra.fr.
Agnès
A
Vallier
Université de Lyon, INSA-Lyon, INRA, UMR203 BF2I, Biologie Fonctionnelle Insectes et Interactions, F-69621, Villeurbanne, France. nicolas.parisot@insa-lyon.fr.
Nicolas
N
Parisot
Université de Lyon, INSA-Lyon, INRA, UMR203 BF2I, Biologie Fonctionnelle Insectes et Interactions, F-69621, Villeurbanne, France. carole.monegat@insa-lyon.fr.
Carole
C
Vincent-Monégat
Université de Lyon, INSA-Lyon, INRA, UMR203 BF2I, Biologie Fonctionnelle Insectes et Interactions, F-69621, Villeurbanne, France. severine.balmand@lyon.inra.fr.
Séverine
S
Balmand
Université de Lyon, CNRS, UMR5558 LBBE, Laboratoire de Biométrie et de Biologie Évolutive, F-69621, Villeurbanne, France. marie-christine.carpentier@univ-perp.fr.
Marie-Christine
MC
Carpentier
Université de Lyon, INSA-Lyon, INRA, UMR203 BF2I, Biologie Fonctionnelle Insectes et Interactions, F-69621, Villeurbanne, France. anna.zaidman@insa-lyon.fr.
Anna
A
Zaidman-Rémy
Université de Lyon, INSA-Lyon, INRA, UMR203 BF2I, Biologie Fonctionnelle Insectes et Interactions, F-69621, Villeurbanne, France. abdelaziz.heddi@insa-lyon.fr.
Abdelaziz
A
Heddi
D000818:Animals; D017209:Apoptosis / Q000235:genetics; D001343:Autophagy / Q000235:genetics; D001419:Bacteria / Q000235:genetics; D001483:Base Sequence; D004064:Digestive System / Q000382:microbiology; D059014:High-Throughput Nucleotide Sequencing; D019476:Insect Proteins / Q000096:biosynthesis / Q000235:genetics*; D007814:Larva / Q000254:growth & development / Q000276:immunology / Q000382:microbiology; D013559:Symbiosis / Q000235:genetics*; D048889:Weevils / Q000235:genetics* / Q000254:growth & development / Q000276:immunology* / Q000382:microbiology
D019476:Insect Proteins