Host and Symbiont Jointly Control Gut Microbiota during Complete Metamorphosis.

Paul R Johnston,Jens Rolff,David S Schneider

doi:10.1371/journal.ppat.1005246

Paul R Johnston, Jens Rolff + Show 1 more

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https://doi.org/10.1371/journal.ppat.1005246

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Abstract

Holometabolous insects undergo a radical anatomical re-organisation during metamorphosis. This poses a developmental challenge: the host must replace the larval gut but at the same time retain symbiotic gut microbes and avoid infection by opportunistic pathogens. By manipulating host immunity and bacterial competitive ability, we study how the host Galleria mellonella and the symbiotic bacterium Enterococcus mundtii interact to manage the composition of the microbiota during metamorphosis. Disenabling one or both symbiotic partners alters the composition of the gut microbiota, which incurs fitness costs: adult hosts with a gut microbiota dominated by pathogens such as Serratia and Staphylococcus die early. Our results reveal an interaction that guarantees the safe passage of the symbiont through metamorphosis and benefits the resulting adult host. Host-symbiont “conspiracies” as described here are almost certainly widespread in holometobolous insects including many disease vectors.

Highlights

The vast majority of animal species are insects [1,2]
Symbionts and Pathogens during Host Metamorphosis organisms (Drosophila melanogaster, Galleria mellonella) with distinct larval and adult stages separated by metamorphosis, which entails dramatic remodeling of external and internal anatomy [3,4]
Using a combination of 16S rRNA gene amplicon sequencing, qPCR, and conventional bacterial culturing we monitored the composition of the gut microbiota during the larval-pupal molt as well as after adult eclosion

Summary

Introduction

The vast majority of animal species are insects [1,2]. Most species of insects are holometabolous, including important vectors of infectious disesases (sandflies, mosquitoes) and modelPLOS Pathogens | DOI:10.1371/journal.ppat.1005246 November 6, 2015Symbionts and Pathogens during Host Metamorphosis organisms (Drosophila melanogaster, Galleria mellonella) with distinct larval and adult stages separated by metamorphosis, which entails dramatic remodeling of external and internal anatomy [3,4]. The vast majority of animal species are insects [1,2]. Most species of insects are holometabolous, including important vectors of infectious disesases (sandflies, mosquitoes) and model. Symbionts and Pathogens during Host Metamorphosis organisms (Drosophila melanogaster, Galleria mellonella) with distinct larval and adult stages separated by metamorphosis, which entails dramatic remodeling of external and internal anatomy [3,4]. The evolutionary advantage of metamorphosis is usually explained by the adaptive decoupling hypothesis [5]: traits in larvae and adults are genetically decoupled, facilitating adaptation to life-stage specific selection [6]. Anatomical re-organization of the body, poses a significant problem during the replacement of the gut, as the gut hosts a microbiota. Either the organism must eradicate and subsequently re-establish the microbiota from the environment, or it must maintain its microbiota while preventing opportunistic microbes from entering the hemocoel and causing infections

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