Proteogenomic reconstruction of organ-specific metabolic networks in an environmental sentinel species, the amphipodGammarus fossarum

Author:

Koenig NatachaORCID,Baa-Puyoulet Patrice,Lafont Amélie,Lorenzo-Colina Isis,Navratil Vincent,Leprêtre Maxime,Sugier Kevin,Delorme Nicolas,Garnero Laura,Queau Hervé,Gaillard Jean-Charles,Kielbasa Mélodie,Ayciriex Sophie,Calevro Federica,Chaumot Arnaud,Charles Hubert,Armengaud Jean,Geffard Olivier,Esposti Davide DegliORCID

Abstract

AbstractMetabolic pathways are targets of environmental contaminants underlying a large variability of toxic effects throughout biodiversity. However, the systematic reconstruction of metabolic pathways remains limited in environmental sentinel species due to the lack of available genomic data in many taxa of animal diversity. In order to improve the knowledge of the metabolism of sentinel species, in this study we used a multi-omics approach to reconstruct the most comprehensive map of metabolic pathways for a crustacean model in biomonitoring, the amphipodGammarus fossarum.We revisited the assembly of RNA-seq data byde novoapproaches drastically reducing RNA contaminants and transcript redundancy. We also acquired extensive mass spectrometry shotgun proteomic data on several organs fromG. fossarummales and females to identify organ-specific metabolic profiles.TheG. fossarummetabolic pathway reconstruction (available through the metabolic database GamfoCyc) was performed by adapting the genomic tool CycADS and we identified 377 pathways representing 7,630 annotated enzymes, 2,610 enzymatic reactions and the expression of 858 enzymes was experimentally validated by proteomics. Our analysis shows organ-specific metabolic profiles, such as an elevated abundance in enzymes involved in ATP biosynthesis and fatty acid beta-oxidation indicative of the high-energy requirement of the gills, or the key anabolic and detoxification role of the hepatopancreatic caeca, as exemplified by the specific expression of the retinoid biosynthetic pathways and glutathione synthesis.In conclusion, the multi-omics data integration performed in this study provides new resources to investigate metabolic processes in crustacean amphipods and their role in mediating the effects of environmental contaminant exposures in sentinel species.

Publisher

Cold Spring Harbor Laboratory

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