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Characterizing and modeling the evolution of host-microbiota interactions

Abstract : A plethora of recent studies have characterized the composition and functional role of microbial communities hosted by animals and plants, called microbiota. The overall goal of my PhD is to advance our understanding of how microbiota evolve with their host species, using data comprised of the phylogenetic relationships between host species and metabarcoding microbial sequences characterizing their microbial communities. We developed new quantitative tools, collected data, and performed a series of analyses, all directed to this common overarching goal. We considered both microbiota-animal and microbiota-plant systems, with a specific focus on mycorrhizal interactions. In Chapter I, we study the evolution of the microbiota during the diversification of host clades. We develop a quantitative approach for inferring the modes of microbial inheritance as host clades diversify. Given a host phylogeny and the microbiota of present-day species, each characterized by a list of short DNA sequences clustered into operational taxonomic units (OTUs), our approach uses nucleotide variability within OTUs to detect OTUs that are vertically transmitted. We apply this approach to two distinct systems, the gut microbiota of primates and a clade of Hawaiian spiders. We find that >5% of bacteria in primate guts are vertically transmitted, whereas there is no evidence of vertical transmission in spiders, confirming that host-microbiota evolutionary dynamics are highly heterogeneous across the animal kingdom. Finally, we compare the performances of our model to other available approaches and find that it is less prone to false-positives when the nucleotide variability within OTUs is low. In Chapter II, we examine the interplay between the evolutionary history of host and host-associated microbial clades. We focus on two specific questions: “To what extent does evolutionary history influence which microbial species interact with which host species?” and “How does the evolutionary history of hosts influence the diversification of host-associated microbial clades?”. The first question leads us to compare different methods for estimating phylogenetic signals in host-microbiota interactions, i.e. whether closely related species share similar sets of partners, with an application on plant-mycorrhizal interactions. We find that one of the most widely used approaches often detects phylogenetic signals when it should not and that Mantel tests perform best. We explore the second question by studying the diversification of the arbuscular mycorrhizal fungi (Glomeromycotina) in the past 500 million years and evaluating how land plants might have affected the diversification of these obligate mycorrhizal symbionts. Our analyses support that these fungi have experienced a recent diversification slowdown that might be linked to the shrinkage of their mycorrhizal niches as plant lineages evolve alternative symbiotic strategies. In Chapter III, we focus on the evolution of cheating in host-microbiota mutualisms, by taking the mycorrhizal symbiosis as a case study. We explore constraints on the evolutionary emergence of cheating in plants (mycoheterotrophy) by analyzing the patterns of plant-mycorrhizal fungus interactions at the global scale. Next, we investigate whether similar constraints are found in local mycorrhizal networks including initially mycoheterotrophic plants (Lycopodiaceae) that we have sampled in La Réunion island. We conclude that there are overall strong constraints limiting the emergence of cheaters in the mycorrhizal symbiosis, but these constraints might be relaxed in the local communities where cheating occurs. Overall, my thesis illustrates how new or recent computational tools, in combination with metabarcoding sequencing data, allow studying how microbiota evolve with their hosts. We discuss the challenges and promise of this comparative approach to host-microbiota evolution.
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Submitted on : Wednesday, December 15, 2021 - 3:14:19 PM
Last modification on : Friday, June 24, 2022 - 3:35:02 AM
Long-term archiving on: : Wednesday, March 16, 2022 - 7:10:15 PM

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Benoît Perez-Lamarque. Characterizing and modeling the evolution of host-microbiota interactions. Microbiology and Parasitology. Université Paris sciences et lettres, 2021. English. ⟨NNT : 2021UPSLE003⟩. ⟨tel-03481801⟩

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