Phenotypic Parallelism during Experimental Adaptation of a Free-Living Bacterium to the Zebrafish Gut

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...

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Autores principales:	Jarrett F. Lebov, Brandon H. Schlomann, Catherine D. Robinson, Brendan J. M. Bohannan
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	bacteriology biofilm ecology evolution genetics genomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e6f0ef2902aa4f0ebc8a24f1dfbcf7bc
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spelling	oai:doaj.org-article:e6f0ef2902aa4f0ebc8a24f1dfbcf7bc2021-11-15T15:56:44ZPhenotypic Parallelism during Experimental Adaptation of a Free-Living Bacterium to the Zebrafish Gut10.1128/mBio.01519-202150-7511https://doaj.org/article/e6f0ef2902aa4f0ebc8a24f1dfbcf7bc2020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01519-20https://doaj.org/toc/2150-7511ABSTRACT 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.Jarrett F. LebovBrandon H. SchlomannCatherine D. RobinsonBrendan J. M. BohannanAmerican Society for MicrobiologyarticlebacteriologybiofilmecologyevolutiongeneticsgenomicsMicrobiologyQR1-502ENmBio, Vol 11, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	bacteriology biofilm ecology evolution genetics genomics Microbiology QR1-502
spellingShingle	bacteriology biofilm ecology evolution genetics genomics Microbiology QR1-502 Jarrett F. Lebov Brandon H. Schlomann Catherine D. Robinson Brendan J. M. Bohannan Phenotypic Parallelism during Experimental Adaptation of a Free-Living Bacterium to the Zebrafish Gut
description	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.
format	article
author	Jarrett F. Lebov Brandon H. Schlomann Catherine D. Robinson Brendan J. M. Bohannan
author_facet	Jarrett F. Lebov Brandon H. Schlomann Catherine D. Robinson Brendan J. M. Bohannan
author_sort	Jarrett F. Lebov
title	Phenotypic Parallelism during Experimental Adaptation of a Free-Living Bacterium to the Zebrafish Gut
title_short	Phenotypic Parallelism during Experimental Adaptation of a Free-Living Bacterium to the Zebrafish Gut
title_full	Phenotypic Parallelism during Experimental Adaptation of a Free-Living Bacterium to the Zebrafish Gut
title_fullStr	Phenotypic Parallelism during Experimental Adaptation of a Free-Living Bacterium to the Zebrafish Gut
title_full_unstemmed	Phenotypic Parallelism during Experimental Adaptation of a Free-Living Bacterium to the Zebrafish Gut
title_sort	phenotypic parallelism during experimental adaptation of a free-living bacterium to the zebrafish gut
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/e6f0ef2902aa4f0ebc8a24f1dfbcf7bc
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Phenotypic Parallelism during Experimental Adaptation of a Free-Living Bacterium to the Zebrafish Gut

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