Host adaptation in gut Firmicutes is associated with sporulation loss and altered transmission cycle

Hilary P Browne,Elisa Viciani,Nicholas J R Dawson,Alexandre Almeida,Samuel C Forster,David Goulding,Nitin Kumar,Anne T Adoum,Claire Cormie,Trevor D Lawley,Kevin Vervier

doi:10.1186/s13059-021-02428-6

Abstract

BackgroundHuman-to-human transmission of symbiotic, anaerobic bacteria is a fundamental evolutionary adaptation essential for membership of the human gut microbiota. However, despite its importance, the genomic and biological adaptations underpinning symbiont transmission remain poorly understood. The Firmicutes are a dominant phylum within the intestinal microbiota that are capable of producing resistant endospores that maintain viability within the environment and germinate within the intestine to facilitate transmission. However, the impact of host transmission on the evolutionary and adaptive processes within the intestinal microbiota remains unknown.ResultsWe analyze 1358 genomes of Firmicutes bacteria derived from host and environment-associated habitats. Characterization of genomes as spore-forming based on the presence of sporulation-predictive genes reveals multiple losses of sporulation in many distinct lineages. Loss of sporulation in gut Firmicutes is associated with features of host-adaptation such as genome reduction and specialized metabolic capabilities. Consistent with these data, analysis of 9966 gut metagenomes from adults around the world demonstrates that bacteria now incapable of sporulation are more abundant within individuals but less prevalent in the human population compared to spore-forming bacteria.ConclusionsOur results suggest host adaptation in gut Firmicutes is an evolutionary trade-off between transmission range and colonization abundance. We reveal host transmission as an underappreciated process that shapes the evolution, assembly, and functions of gut Firmicutes.

Highlights

Human-to-human transmission of symbiotic, anaerobic bacteria is a fundamental evolutionary adaptation essential for membership of the human gut microbiota
Co-evolution between humans and these symbiotic, anaerobic bacteria requires that individual bacterial taxa faithfully and efficiently transmit and colonize, as an inability to do either leads to extinction from the indigenous microbiota [5,6,7,8]
In this study, combining large-scale genomic analysis with phenotypic validation of human gut bacteria from the Firmicutes phylum, we show that sporulation loss is associated with signatures of host adaptation such as genome reduction and more specialized metabolic capabilities

Summary

Introduction

Human-to-human transmission of symbiotic, anaerobic bacteria is a fundamental evolutionary adaptation essential for membership of the human gut microbiota. Despite its importance, the genomic and biological adaptations underpinning symbiont transmission remain poorly understood. The impact of host transmission on the evolutionary and adaptive processes within the intestinal microbiota remains unknown. Co-evolution between humans and these symbiotic, anaerobic bacteria requires that individual bacterial taxa faithfully and efficiently transmit and colonize, as an inability to do either leads to extinction from the indigenous microbiota [5,6,7,8]. Key adaptations of symbiotic bacteria in human populations, require coordination of colonization and transmission functions. The transmission cycle of gut bacteria is underpinned by a deep evolutionary selection that remains poorly understood

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Conclusion