Multiscale Evolutionary Dynamics of Host-Associated Microbiomes

Abstract

The composite members of the microbiota face a range of selective pressures and must adapt to persist in the host. We highlight recent work characterizing the evolution and transfer of genetic information across nested scales of host-associated microbiota, which enable resilience to biotic and abiotic perturbations. At the strain level, we consider the preservation and diversification of adaptive information in progeny lineages. At the community level, we consider genetic exchange between distinct microbes in the ecosystem. Finally, we frame microbiomes as open systems subject to acquisition of novel information from foreign ecosystems through invasion by outsider microbes.

Keywords: clonal interference; colonization; ecology; genomics; horizontal gene transfer; human microbiome; microbial evolution; microbial transmission; pathogen invasion; xenobiotics.

Figure 1. Scales of Microbial Evolution

A) Scale 1: evolution via single nucleotide polymorphisms, rearrangements, and transposon-mediated insertions. B) Scale 2: evolution within a microbiome, encompassing horizontal gene transfer mediated by phage, conjugation, and transformation. C) Scale 3: evolution between microbial communities is mediated by organismal transfer.

Figure 2. Features of the Human Body Impacting Microbial Evolution

The selective pressures governing microbial evolution are often dictated by unique features of the habitat in which it occurs, including its nutrient sources, microbial density, dilution rate, and spatial arrangement.

Figure 3. Evolutionary dynamics of co-localized and competing lineages

A) An example of adaptive dynamics involving antibiotic producing, sensitive, resistant, or degrader microbial phenotypes. Dynamics of a co-evolutionary arms race between lineages or species with inhibitory interactions is driven by cycles of fitness advantage and fitness cost, and by the emergence of new lineages with evolved phenotypes. B) Left: The classical dominant-lineage model of evolution. Neutral variation accumulates until a bottleneck event leads to a hard sweep resulting in allelic fixation. A new dominant lineage is established (black lines), and less fit lineages fall to extinction (grey lines). The background colors denote relative abundances of specific lineages. Right: The clonal interference model of evolution. Adaptive and polymorphic mutations arise in parallel, and lineages compete and co-exist over prolonged periods.

Figure 4. Future directions in studying evolution of host-associated microbes in situ

A fundamental challenge in studying the evolution of individual microbes within communities remains the ability to associate polymorphism with a specific lineage over time. Three approaches to overcoming this barrier that have been subject to great recent advances are metagenomics assembly (A), next-generation culturing (B), and single-cell sequencing (C).