Genes Activated by
            <i>Vibrio cholerae</i>
            upon Exposure to
            <i>Caenorhabditis elegans</i>
            Reveal the Mannose-Sensitive Hemagglutinin To Be Essential for Colonization

List, Cornelia; Grutsch, Andreas; Radler, Claudia; Çakar, Fatih; Zingl, Franz G.; Schild-Prüfert, Kristina; Schild, Stefan

doi:10.1128/mspheredirect.00238-18

Cited by 16 publications

(15 citation statements)

References 44 publications

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“…Interestingly, the Msh pilus has been shown to play a role in a number of other host-microbe systems. For instance, within the Vibrio genus, Msh pili have been suggested to be important for adherence to human intestinal cells ( 33 ), as well as colonization of the digestive tract of Caenorhabditis elegans ( 34 ), and the light organ of Euprymna tasmanica ( 35 ). In addition, in both Vibrio and Pseudomonas systems, evidence suggests this pilus can interact with components of the mammalian immune system ( 12 , 36 ).…”

Section: Resultsmentioning

confidence: 99%

“…Each point represents the competitive index measured for a single biological replicate. (33), as well as colonization of the digestive tract of Caenorhabditis elegans (34), and the light organ of Euprymna tasmanica (35). In addition, in both Vibrio and Pseudomonas systems, evidence suggests this pilus can interact with components of the mammalian immune system (12,36).…”

Section: Figmentioning

confidence: 99%

See 1 more Smart Citation

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

Lebov

Schlomann

Robinson

et al. 2020

mBio

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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.

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Section: Resultsmentioning

confidence: 99%

Section: Figmentioning

confidence: 99%

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

Lebov

Schlomann

Robinson

et al. 2020

mBio

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“…13 Previous studies have revealed virulence-associated factors involved in the pathogenicity of V. cholerae, including zonula occludens toxin (zot), accessory cholera enterotoxin (ace), El Tor hemolysin (hlyA), hemagglutinin protease (hapA), RTX toxin (rtxCABD), thermolabile hemolysin (tlh), mannose-sensitive hemagglutination (MSHA; mshA), and putative type IV pilus ( pilA). [14][15][16][17][18] Therefore, continuous detection of the non-O1/ 0139 V. cholerae in aquatic products is also crucial for food safety systems.…”

Section: Introductionmentioning

confidence: 99%

Virulence, Resistance, and Genomic Fingerprint Traits ofVibrio choleraeIsolated from 12 Species of Aquatic Products in Shanghai, China

Pan

Liang

et al. 2020

Microbial Drug Resistance

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Vibrio cholerae is a waterborne bacterium and can cause epidemic cholera disease worldwide. Continuous monitoring of V. cholerae contamination in aquatic products is imperative for assuring food safety. In this study, we determined virulence, antimicrobial susceptibility, heavy metal tolerance, and genomic fingerprints of 370 V. cholerae isolates recovered from 12 species of commonly consumed aquatic products collected from July to September of 2018 in Shanghai, China. Among the species, Leiocassis longirostris, Ictalurus punetaus, Ophiocephalus argus Cantor, and Pelteobagrus fulvidraco were for the first time detected for V. cholerae. Toxin genes ctxAB, tcpA, ace, and zot were absent from all the V. cholerae isolates. However, high occurrence of virulence-associated genes was detected, such as hapA (82.7%), hlyA (81.4%), rtxCABD (81.4%, 24.3%, 80.3%, and 80.8%, respectively), and tlh (80.5%). Approximately 62.2% of the 370 V. cholerae isolates exhibited resistance to streptomycin, followed by ampicillin (60.3%), rifampicin (53.8%), trimethoprim (38.4%), and sulfamethoxazole-trimethoprim (37.0%). Moreover, *57.6% of the isolates showed multidrug resistant phenotypes with 57 resistance profiles, which was significantly different among the 12 species (multiple antimicrobial resistance index, p < 0.001). Meanwhile, high incidence of tolerance to heavy metals Hg 2+ (69.5%), Ni 2+ (32.4%), and Cd 2+ (30.8%) was observed among the isolates. The enterobacterial repetitive intergenic consensus-polymerase chain reaction (ERIC-PCR)-based fingerprinting profiles classified the 370 V. cholerae isolates into 239 different ERIC-genotypes, which demonstrated diverse genomic variation among the isolates. Overall, the results in this study meet the increasing need of food safety risk assessment of aquatic products.

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“…Interestingly, the msh pilus has been shown to play a role in a number of other host-microbe systems. For instance, within the Vibrio genus, msh pili have been suggested to be important for adherence to human intestinal cells [33], as well as colonization of the digestive tract of Caenorhabditis elegans [34], and the light organ of Euprymna tasmanica [35]. Additionally, in both Vibrio and Pseudomonas systems, evidence suggests this pilus can interact with components of the mammalian immune system [12, 36].…”

Section: Resultsmentioning

confidence: 99%

Phenotypic parallelism during experimental adaptation of a free-living bacterium to the zebrafish gut

Lebov

Schlomann

Robinson

et al. 2020

Preprint

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31Despite the fact that animals encounter a plethora of bacterial species throughout their lives, only 32 a subset are capable of colonizing vertebrate digestive tracts, and these bacteria can profoundly 33 influence the health and development of their animal hosts. However, it is still unknown how 34 bacteria evolve symbioses with animal hosts, and this process is central to both the assembly and 35 function of gut bacterial communities. Therefore, we used experimental evolution to study a 36 free-living bacterium as it adapts to a novel vertebrate host. We serially passaged replicate 37 populations of Shewanella oneidensis, through the digestive tracts of larval zebrafish (Danio 38 rerio). After only 20 passages, representing approximately 200 bacterial generations, isolates 39 from replicate evolved populations displayed an improved ability to colonize larval zebrafish 40 digestive tracts during competition against their unpassaged ancestor. Upon sequencing the 41 genomes of these evolved isolates, we discovered that the two isolates with the highest mean 42 competitive fitness accumulated unique sets of mutations. We characterized the swimming 43 motility and aggregation behavior of these isolates, as these phenotypes have previously been 44 shown to alter host-microbe interactions. Despite exhibiting different biofilm characteristics, 45 both isolates evolved augmented swimming motility. These enhancements are consistent with 46 expectations based on the behavior of a closely related Shewanella strain previously isolated 47 Introduction: 54 Bacterial lineages have radiated into practically every imaginable niche on Earth [1, 2]. 55In particular, the vertebrate digestive tract houses bacterial communities whose composition is 56 distinct from those found in surrounding environments [3, 4], and this suggests that host-57 associated bacteria maintain certain traits that enable them to colonize animal hosts. In order to 58 establish and maintain host-association, bacteria must surmount a multitude of complex 59 challenges, including traversing diverse physical landscapes, harvesting energy from dynamic 60 nutrient sources, and protecting themselves from antimicrobial compounds. Thus, the number of 61 traits involved in host-association is likely enormous [5, 6]. Despite this complexity, previous 62 analyses indicate that novel host-microbe symbioses have arisen multiple times throughout 63 evolutionary history [7]. However, it is unknown which suites of traits enable bacteria to 64 transition to host association, or how likely they are to evolve. 65It is well established that bacteria residing in vertebrate digestive tracts have substantial 66 impacts on the health and development of their animal hosts [8][9][10][11]. Consequently, many 67 researchers have sought to understand which traits provide bacteria the capacity to colonize the 68 vertebrate gut [12][13][14][15][16][17], but this body of work has relied almost exclusively on snapshots of host-69 microbe relationships after they have evolved. Because...

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Genes Activated by Vibrio cholerae upon Exposure to Caenorhabditis elegans Reveal the Mannose-Sensitive Hemagglutinin To Be Essential for Colonization

Cited by 16 publications

References 44 publications

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

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

Virulence, Resistance, and Genomic Fingerprint Traits ofVibrio choleraeIsolated from 12 Species of Aquatic Products in Shanghai, China

Phenotypic parallelism during experimental adaptation of a free-living bacterium to the zebrafish gut

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