Spatial Metabolomics Reveals the Multifaceted Nature of Lamprey Buccal Gland and Its Diverse Mechanisms for Blood-Feeding

Abstract

Lampreys are blood-sucking vampires in marine environments. From a survival perspective, it is expected that the lamprey buccal gland exhibits a repository of pharmacologically active components to modulate the host’s homeostasis, inflammatory and immune responses. By analyzing the metabolic profiles of 14 different lamprey tissues, we show that two groups of metabolites in the buccal gland of lampreys, prostaglandins and the kynurenine pathway metabolites, can be injected into the host fish to assist lamprey blood feeding. Prostaglandins are well-known blood-sucking-associated metabolites that act as vasodilators and anticoagulants to maintain vascular homeostasis and are involved in inflammatory responses. The vasomotor reactivity test on catfish aortic ring showed that kynurenine can also relax the blood vessels of the host fish, thus improving the blood flow of the host fish at the bite site. Finally, a lamprey spatial metabolomics database (https://www.lampreydb.com) was constructed to assist studies using lampreys as animal model.

A spatial metabolomics study of the lampreys leads to the identification of the kynurenine pathway metabolites and prostaglandins in their buccal gland secretions (saliva), which are likely involved in promoting blood flow when feeding on host fishes.