Abstract
Although animals encounter a plethora of bacterial species throughout their lives, only a subset colonize vertebrate digestive tracts, and these bacteria can profoundly influence the health and development of their animal hosts. However, our understanding of how bacteria initiate symbioses with animal hosts remains underexplored, and this process is central to the assembly and function of gut bacterial communities. Therefore, we used experimental evolution to study a free-living bacterium as it adapts to a novel vertebrate host by serially passaging replicate populations of Shewanella oneidensis through the intestines of larval zebrafish (Danio rerio). After approximately 200 bacterial generations, isolates from evolved populations improved their ability to colonize larval zebrafish during competition against their unpassaged ancestor. Genome sequencing revealed unique sets of mutations in the two evolved isolates exhibiting the highest mean competitive fitness. One isolate exhibited increased swimming motility and decreased biofilm formation compared to the ancestor, and we identified a missense mutation in the mannose-sensitive hemagglutinin pilus operon that is sufficient to increase fitness and reproduce these phenotypes. The second isolate exhibited enhanced swimming motility but unchanged biofilm formation, and here the genetic basis for adaptation is less clear. These parallel enhancements in motility and fitness resemble the behavior of a closely related Shewanella strain previously isolated from larval zebrafish and suggest phenotypic convergence with this isolate. Our results demonstrate that adaptation to the zebrafish gut is complex, with multiple evolutionary pathways capable of improving colonization, but that motility plays an important role during the onset of host association.IMPORTANCE Although animals encounter many bacterial species throughout their lives, only a subset colonize vertebrate digestive tracts, and these bacteria can profoundly influence the health and development of their animal hosts. We used experimental evolution to study a free-living bacterium as it adapts to a novel vertebrate host by serially passaging replicate populations of Shewanella oneidensis through the intestines of larval zebrafish (Danio rerio). Our results demonstrate that adaptation to the zebrafish gut is complex, with multiple evolutionary pathways capable of improving colonization, but that motility plays an important role during the onset of host association.
Highlights
Bacterial lineages have radiated into practically every imaginable niche on Earth [1, 2].In particular, the vertebrate digestive tract houses bacterial communities whose composition is distinct from those found in surrounding environments [3, 4], and this suggests that hostassociated bacteria maintain certain traits that enable them to colonize animal hosts
The vertebrate digestive tract houses bacterial communities whose composition is distinct from those found in surrounding environments [3, 4], and this suggests that hostassociated bacteria maintain certain traits that enable them to colonize animal hosts
MR-1 colonizes zebrafish at lower densities than a closely-related Shewanella zebrafish isolate: Gut-associated bacteria are routinely isolated from their animal hosts
Summary
The vertebrate digestive tract houses bacterial communities whose composition is distinct from those found in surrounding environments [3, 4], and this suggests that hostassociated bacteria maintain certain traits that enable them to colonize animal hosts. The number of traits involved in host-association is likely enormous [5, 6]. Despite this complexity, previous analyses indicate that novel host-microbe symbioses have arisen multiple times throughout evolutionary history [7]. Previous analyses indicate that novel host-microbe symbioses have arisen multiple times throughout evolutionary history [7] It is unknown which suites of traits enable bacteria to transition to host association, or how likely they are to evolve
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