Formicine ants swallow their highly acidic poison for gut microbial selection and control

Abstract

Animals continuously encounter microorganisms that are essential for health or cause disease. They are thus challenged to control harmful microbes while allowing the acquisition of beneficial microbes. This challenge is likely especially important for social insects with respect to microbes in food, as they often store food and exchange food among colony members. Here we show that formicine ants actively swallow their antimicrobial, highly acidic poison gland secretion. The ensuing acidic environment in the stomach, the crop, can limit the establishment of pathogenic and opportunistic microbes ingested with food and improve the survival of ants when faced with pathogen contaminated food. At the same time, crop acidity selectively allows acquisition and colonization by Acetobacteraceae, known bacterial gut associates of formicine ants. This suggests that swallowing of the poison in formicine ants acts as a microbial filter and that antimicrobials have a potentially widespread but so far underappreciated dual role in host-microbe interactions.

Biomarkers in a socially exchanged fluid reflect colony maturity, behavior, and distributed metabolism

“…These significant lysosomal signatures we see in trophallactic fluid may indicate the mechanism of secretion ( Martínez et al, 2020 ), or may give us cues of how this fluid has evolved. As trophallactic fluid has become acidified in formicine ants ( Tragust et al, 2020 ), lysosomal genes could have been duplicated and neofunctionalized to a new role in this acidic fluid, similarly to juvenile-hormone-esterase-like proteins in trophallactic fluid ( LeBoeuf et al, 2018 ). The fact that many abundant trophallactic fluid proteins represent clusters of related proteins from a few families (cathepsins, guanine deaminases, maltases) suggests there has been adaptive evolution in the proteins arriving in this fluid.…”

Partner fidelity and environmental filtering preserve stage‐specific turtle ant gut symbioses for over 40 million years

“…Partner fidelity is the most widely documented, being evidenced by the many symbionts passaged to offspring through transovarial transfer (Koga et al, 2012; Luan et al, 2016), or a range of “out‐of‐body” mechanisms (Salem et al, 2015). But many insects acquire symbionts from the environment, retaining specific subsets of the inoculated microbes (Birer et al, 2020; Chandler et al, 2011; Jones et al, 2019; Ravenscraft et al, 2019) due to their physiology and behavior (Engel & Moran, 2013; Tragust et al, 2020), or the actions of their regular symbiont partners (Itoh et al, 2019; Worsley et al, 2021). Among those adopting such environmental filtering mechanisms, some have evolved means for partner choice, selecting beneficial microbial partners amid a broader set of symbiotic suitors (Ohbayashi et al, 2015).…”

8-HQA adjusts the number and diversity of bacteria in the gut microbiome of Spodoptera littoralis

“…Some insects employ their innate immune pathways for regulating bacterial populations, for example green weevils and their antimicrobial peptides (AMP; Login et al, 2011 ). Formicine ants swallow their acidic antimicrobial gland secretion to keep opportunistic pathogens in check ( Tragust et al, 2020 ).…”