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.
Highlights
Animals commonly harbor gut associated microbial communities (Engel and Moran, 2013, Moran et al, 2019)
We first investigate whether the poison is swallowed during acidopore grooming in 88 C. floridanus and seven other formicine ant species from three genera in a comparative survey through measurement of pH levels in the crop and midgut lumen, experimental manipulation of acidopore access, and behavioural observations
In loss of acidopore and poison access during survival experiments and in in vitro and in vivo bacterial viability and growth experiments, we investigate whether swallowing of the poison can serve gut microbial control and prevent bacterial pathogen infection analogous to acidic stomachs of higher vertebrates and acidic midgut regions in the fruit fly
Summary
Animals commonly harbor gut associated microbial communities (Engel and Moran, 2013, Moran et al, 2019). Patterns of recurring gut microbial communities have been described for many animal groups (Brune and Dietrich, 2015, Kwong et al, 2017, Ochman et al, 2010). The processes generating these patterns are often not well understood. Food is an important environmental source of microbial gut associates (Blum et al, 2013, Broderick and Lemaitre, 2012, David et al, 2014, Hammer et al, 2017, Perez-Cobas et al, 2015) and poses a challenge, the need to discriminate between harmful and beneficial microbes, as food may contain microbes that produce toxic chemicals or that are pathogenic (Burkepile et al, 2006, Demain and Fang, 2000, Janzen, 1977, Trienens et al, 2010). While trophallaxis can facilitate the transmission of beneficial microbes, from an epidemiological perspective it can entail significant costs, as it might open the door to unwanted microbial opportunists and pathogens that can take advantage of these transmission routes (Onchuru et al, 2018, Salem et al, 2015)
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