The Drosophila gut: A gatekeeper and coordinator of organism fitness and physiology

Abstract

Multicellular organisms have evolved organs and tissues with highly specialized tasks. For instance, nutrients are assimilated by the gut, sensed, processed, stored, and released by adipose tissues and liver to provide energy consumed by peripheral organ activities. The function of each organ is modified by local clues and systemic signals derived from other organs to ensure a coordinated response accommodating the physiological needs of the organism. The intestine, which represents one of the largest interfaces between the internal and external environment, plays a key role in sensing and relaying environmental inputs such as nutrients and microbial derivatives to other organs to produce systemic responses. In turn, gut physiology and immunity are regulated by multiple signals emanating from other organs including the brain and the adipose tissues. In this review, we highlight physiological processes where the gut serves as a key organ in coupling systemic signals or environmental cues with organism growth, metabolism, immune activity, aging, or behavior. Robust strategies involving intraorgan and interorgan signaling pathways have evolved to preserve gut size in homeostatic conditions and restrict growth during damage-induced regenerative phases. Here we review some of the mechanisms that maintain gut size homeostasis and point out known examples of homeostasis-breaking events that promote gut plasticity to accommodate changes in the external or internal environment.

Regulation of Body Size and Growth Control

“…Like juvenile growth, adult growth is influenced by physiological needs and environmental cues. For example, mating induces growth in the reproductive systems of both males and females, and the adult gut undergoes remodeling in response to environmental conditions, mating, and infection to maintain tissue homeostasis ( Leiblich et al 2012 , 2019 ; Ameku and Niwa 2016 ; Ameku et al 2018 ; Colombani and Andersen 2020 ). Adult tissue growth and oogenesis are governed by cell-intrinsic and systemic mechanisms similar to those of juveniles, including TOR, insulin and ecdysone, juvenile hormone (JH), cytokines, TNF-α, and transforming growth factor-β (TGF-β) ( Petryk et al 2003 ; Ono et al 2006 ; Knapp and Sun 2017 ; Colombani and Andersen 2020 ).…”

Integrative developmental ecology: a review of density-dependent effects on life-history traits and host-microbe interactions in non-social holometabolous insects

“…Furthermore, microbes also interact with insect host to modulate adult oviposition behaviour (Jose et al 2019), foraging (Wong et al 2017), reproductive success (Morimoto et al 2017b) and potentially mate choice (Sharon et al 2011) [but see (Leftwich et al 2017)]. Microbes are therefore the 'gatekeepers of organism fitness' (Colombani and Andersen 2020).…”

The gut hormone Allatostatin C regulates food intake and metabolic homeostasis under nutrient stress

“…The gut has emerged as a central signal-integrating regulator of whole-body energy homeostasis. Despite the evolutionary divergence of flies and humans, the guts of these animals exhibit physiological and structural similarity, with the Drosophila midgut functioning analogously to the human small intestine 6,7 . Work in mammals and Drosophila has shown that the gut integrates nutritional and microbiotic cues and converts these into hormonal signals that relay nutritional information systemically to other tissues.…”