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Abstract
BackgroundThe relatively fast selection of symbiotic bacteria within hosts and the potential transmission of these bacteria across generations of hosts raise the question of whether interactions between host and bacteria support emergent adaptive capabilities beyond those of germ-free hosts.ResultsTo investigate possibilities for emergent adaptations that may distinguish composite host-microbiome systems from germ-free hosts, we introduce a population genetics model of a host-microbiome system with vertical transmission of bacteria. The host and its bacteria are jointly exposed to a toxic agent, creating a toxic stress that can be alleviated by selection of resistant individuals and by secretion of a detoxification agent (“detox”). We show that toxic exposure in one generation of hosts leads to selection of resistant bacteria, which in turn, increases the toxic tolerance of the host’s offspring. Prolonged exposure to toxin over many host generations promotes anadditional form of emergent adaptation due to selection of hosts based on detox produced by their bacterial community as a whole (as opposed to properties of individual bacteria).ConclusionsThese findings show that interactions between pure Darwinian selections of host and its bacteria can give rise to emergent adaptive capabilities, including Lamarckian-like adaptation of the host-microbiome system.ReviewersThis article was reviewed by Eugene Koonin, Yuri Wolf and Philippe Huneman.
Highlights
The relatively fast selection of symbiotic bacteria within hosts and the potential transmission of these bacteria across generations of hosts raise the question of whether interactions between host and bacteria support emergent adaptive capabilities beyond those of germ-free hosts
We evaluate the adaptation of host and vertically-transmitted bacteria, which are jointly exposed to a toxic agent
General considerations of the model We consider the simple case of a host-microbiome system in which every host is associated with a single species of bacteria that is transmitted to the host's offspring with perfect fidelity
Summary
The relatively fast selection of symbiotic bacteria within hosts and the potential transmission of these bacteria across generations of hosts raise the question of whether interactions between host and bacteria support emergent adaptive capabilities beyond those of germ-free hosts. We show that the interaction between the selections of host and bacteria can give rise to an emergent, Lamarckian-like adaptation of the host-microbiome system within a single host generation This effect is mediated by distinct modes of stress alleviation and it has non-trivial dependence on the environmental conditions and the traits of the system. Persistence of the exposure over timescales longer than a host generation promotes additional selection of hosts containing bacterial communities, which secrete higher average detox per bacterium (in contrast to selection of individual bacteria, which takes place on much shorter timescales). This gives rise to a second mode of emergent adaptation that is independent of the Lamarckian-like adaptation within a host generation. These alterations promote an increase in toxin tolerance which persists over periods longer than a host generation but shorter than typical evolutionary timescales of the host
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