The gut microbiome buffers dietary adaptation in Bronze Age domesticated dogs

Florencia Debandi,Riccardo Helg,Courtney A Hofman,Simone Rampelli,Elena Biagi,Silvia Turroni,Alberto Taddia,Stephanie L Schnorr,Marco Candela,Maurizio Cattani,Antton Alberdi,Federica D'Amico,Patrizia Brigidi

doi:10.1016/j.isci.2021.102816

Florencia Debandi, Riccardo Helg + Show 11 more

Open Access

https://doi.org/10.1016/j.isci.2021.102816

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Abstract

SummaryIn an attempt to explore the role of the gut microbiome during recent canine evolutionary history, we sequenced the metagenome of 13 canine coprolites dated ca. 3,600–3,450 years ago from the Bronze Age archaeological site of Solarolo (Italy), which housed a complex farming community. The microbiome structure of Solarolo dogs revealed continuity with that of modern dogs, but it also shared some features with the wild wolf microbiome, as a kind of transitional state between them. The dietary niche, as also inferred from the microbiome composition, was omnivorous, with evidence of consumption of starchy agricultural foods. Of interest, the Solarolo dog microbiome was particularly enriched in sequences encoding alpha-amylases and complemented a low copy number of the host amylase gene. These findings suggest that Neolithic dogs could have responded to the transition to a starch-rich diet by expanding microbial functionalities devoted to starch catabolism, thus compensating for delayed host response.

Highlights

SUMMARY In an attempt to explore the role of the gut microbiome during recent canine evolutionary history, we sequenced the metagenome of 13 canine coprolites dated ca. 3,600–3,450 years ago from the Bronze Age archaeological site of Solarolo (Italy), which housed a complex farming community
The microbiome structure of Solarolo dogs revealed continuity with that of modern dogs, but it shared some features with the wild wolf microbiome, as a kind of transitional state between them
Mammals live in close association with mutualistic microbial communities, called microbiomes, which have become integral to host physiology (McFall-Ngai et al, 2013; Moeller et al, 2016)

Summary

Introduction

Mammals live in close association with mutualistic microbial communities, called microbiomes, which have become integral to host physiology (McFall-Ngai et al, 2013; Moeller et al, 2016). An adaptive scenario for host-microbiome complementarity is the GM-mediated acquisition of new functional processes that enable the host to extract more energy, in the form of SCFAs, from otherwise refractory food substrates, expanding the accessible dietary niche (Moeller and Sanders, 2020). This mechanism, which has been important to the evolutionary history of certain animal-microbe symbiotic relationships, probably played an important role in the concomitant ecological shifts throughout the domestication process. Compared with their wild counterparts, domesticated animals show relevant variations in the GM structure (McKenzie et al, 2017; Metcalf et al, 2017; Reese et al, 2021), and this is likely the result of an adaptive response to changes in diet, lifestyle, and physiology (Alberdi et al, 2016; Coelho et al, 2018)

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