Microbiome interactions shape host fitness

Abstract

Gut bacteria can affect key aspects of host fitness, such as development, fecundity, and lifespan, while the host, in turn, shapes the gut microbiome. However, it is unclear to what extent individual species versus community interactions within the microbiome are linked to host fitness. Here, we combinatorially dissect the natural microbiome of Drosophila melanogaster and reveal that interactions between bacteria shape host fitness through life history tradeoffs. Empirically, we made germ-free flies colonized with each possible combination of the five core species of fly gut bacteria. We measured the resulting bacterial community abundances and fly fitness traits, including development, reproduction, and lifespan. The fly gut promoted bacterial diversity, which, in turn, accelerated development, reproduction, and aging: Flies that reproduced more died sooner. From these measurements, we calculated the impact of bacterial interactions on fly fitness by adapting the mathematics of genetic epistasis to the microbiome. Development and fecundity converged with higher diversity, suggesting minimal dependence on interactions. However, host lifespan and microbiome abundances were highly dependent on interactions between bacterial species. Higher-order interactions (involving three, four, and five species) occurred in 13–44% of possible cases depending on the trait, with the same interactions affecting multiple traits, a reflection of the life history tradeoff. Overall, we found these interactions were frequently context-dependent and often had the same magnitude as individual species themselves, indicating that the interactions can be as important as the individual species in gut microbiomes.

Document Details

Document Type
Pub Defense Publication
Publication Date
Dec 03, 2018
Source ID
10.1073/pnas.1809349115

Entities

People

  • Alex Gavryushkin
  • Alison L Gould
  • Benjamin Obadia
  • Eric W. Jones
  • Jean M. Carlson
  • Lisa Lamberti
  • Niko Beerenwinkel
  • Nikolaos Korasidis
  • Vivian Zhang
  • William B Ludington

Organizations

  • Army Research Office
  • Carnegie Institution for Science
  • David and Lucile Packard Foundation
  • ETH Zurich
  • Johns Hopkins University
  • National Science Foundation
  • Office of the Director
  • Royal Society Te Apārangi
  • SIB Swiss Institute of Bioinformatics
  • University of California, Santa Barbara
  • University of Otago
  • William K Bowes Jr Foundation

Tags

Fields of Study

  • Biology
  • Environmental science

Readers

  • Aquatic Ecology
  • Gulf War Illness and Chronic Multisymptom Illness in Veterans.
  • Systems Analysis and Design

Technology Areas

  • Biotechnology