Flagellar Genes Are Associated with the Colonization Persistence Phenotype of the Drosophila melanogaster Microbiota

Morgan, Sarah J; Chaston, John M.

doi:10.1128/spectrum.04585-22

Cited by 9 publications

(10 citation statements)

References 51 publications

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“…Importantly, the other recent studies further support the role of MprF in microbiota persistence in the gut. For example, a metagenome-wide association (MGWA) study identified multiple bacterial genes, including mprF , that are significantly correlated with the level of colonization [69]. Subsequent analyses confirmed that an mprF transposon insertion mutant of Acetobacter fabarum showed decreased persistence within the flies [69].…”

Section: Discussionmentioning

confidence: 99%

MprF-mediated immune evasion is necessary forLactiplantibacillus plantarumresilience inDrosophilagut during inflammation

Arias-Rojas,

Arifah,

Angelidou

et al. 2024

Preprint

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BackgroundMultiple peptide resistance factor (MprF) confers resistance to cationic antimicrobial peptides (AMPs) in several pathogens, thereby enabling evasion of the host immune response. While MprF has been proven to be crucial for the virulence of various pathogens, its role in commensal gut bacteria remains uncharacterized. To close this knowledge gap, we used a common gut commensal of animals,Lactiplantibacillus plantarum, and its natural host, the fruit flyDrosophila melanogaster, as an experimental model to investigate the role of MprF in commensal-host interactions.ResultsTheL. plantarumΔmprFmutant that we generated exhibited deficiency in the synthesis of lysyl-phosphatidylglycerol (Lys-PG), resulting in increased negative cell surface charge and increased susceptibility to AMPs. Susceptibility to AMPs had no effect on ΔmprFmutant’s ability to colonize guts of uninfected flies. However, we observed significantly reduced abundance of the ΔmprFmutant after infection-induced inflammation in the guts of wild-type flies but not flies lacking AMPs. These results demonstrate that host AMPs reduce the abundance of the ΔmprFmutant during infection. We found in addition that the ΔmprFmutant compared to wild-typeL. plantaruminduces a stronger intestinal immune response in flies due to the increased release of immunostimulatory peptidoglycan fragments, indicating an important role of MprF in promoting host tolerance to commensals.ConclusionOverall, our results demonstrate that MprF, besides its well-characterized role in pathogen immune evasion and virulence, is also an important resilience factor in maintaining stable microbiota-host interactions during intestinal inflammation.

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Section: Discussionmentioning

confidence: 99%

MprF-mediated immune evasion is necessary forLactiplantibacillus plantarumresilience inDrosophilagut during inflammation

Arias-Rojas,

Arifah,

Angelidou

et al. 2024

Preprint

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“…These studies have revealed the diversity, composition, dynamics, and functions of microbial communities associated with flies. Recent studies have taken advantage of transposon sequencing techniques to identify microbiome factors important for colonization and impacts on the host (44–47). Of note, similar to our study, flagellar genes were identified as important colonization determinants of one microbiome member Acetobacter fabarum (47), suggesting this may be a common feature for bacterial persistence in the fly gut.…”

Section: Discussionmentioning

confidence: 99%

“…Recent studies have taken advantage of transposon sequencing techniques to identify microbiome factors important for colonization and impacts on the host (44–47). Of note, similar to our study, flagellar genes were identified as important colonization determinants of one microbiome member Acetobacter fabarum (47), suggesting this may be a common feature for bacterial persistence in the fly gut. Our previous work and other reports have highlighted a role for the microbiota in modulating enteric infection by bacteria, yeast, and viruses (48–52).…”

Section: Discussionmentioning

confidence: 99%

Massively parallel mutant selection identifies genetic determinants ofPseudomonas aeruginosacolonization ofDrosophila melanogaster

Miles,

Lozano,

Rajendhran

et al. 2023

Preprint

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Pseudomonas aeruginosais recognized for its ability to colonize diverse habitats and cause disease in a variety of hosts, including plants, invertebrates, and mammals. Understanding how this bacterium is able to occupy wide-ranging niches is important for deciphering its ecology. We used transposon sequencing (Tn-Seq, also known as INSeq) to identify genes inP. aeruginosathat contribute to fitness during colonization ofDrosophila melanogaster. Our results reveal a suite of critical factors, including those that contribute to polysaccharide production, DNA repair, metabolism, and respiration. Comparison of candidate genes with fitness determinants discovered in previous studies ofP. aeruginosaidentified several genes required for colonization and virulence determinants that are conserved across hosts and tissues. This analysis provides evidence for both the conservation of function of several genes across systems, as well as host-specific functions. These findings, which represent the first use of transposon sequencing of a gut pathogen inDrosophila, demonstrate the power of Tn-Seq in the fly model system and advance existing knowledge of intestinal pathogenesis byD. melanogaster,revealing bacterial colonization determinants that contribute to a comprehensive portrait ofP.aeruginosalifestyles across habitats.ImportanceDrosophila melanogasteris a powerful model for understanding host-pathogen interactions. Research with this system has yielded notable insights into mechanisms of host immunity and defense, many of which emerged from analysis of bacterial mutants defective for well-characterized virulence factors. These foundational studies – and advances in high-throughput sequencing of transposon mutants – support unbiased screens of bacterial mutants in the fly. To investigate mechanisms of host-pathogen interplay and exploit the tractability of this model host, we used a high-throughput, genome-wide mutant analysis to find genes that enable a pathogen,P. aeruginosa, to colonize the fly. Our analysis reveals critical mediators ofP. aeruginosaestablishment in its host, some of which are required across fly and mouse systems. These findings demonstrate the utility of massively parallel mutant analysis and provide a platform for aligning the fly toolkit with comprehensive bacterial genomics.

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“…In laboratory conditions, bacteria have been widely investigated for their ability to swim towards resources [11,12], display quorum sensing [13], or swim away from toxins [14]. Several experimental studies show that the hydration level of surfaces generally predicts how easily bacteria can colonize a given surface [15], and that flagellar motility also predicts the temporal persistence of bacterial pathogens in host microbiomes [16]. The high energetic cost of powering the flagellar machinery is tightly linked to regulatory systems that control flagellar expression depending on the spatial proximity and quality of available resources (i.e., optimal foraging based on energetic constraints; [17][18][19]).…”

Section: Introductionmentioning

confidence: 99%

The ecological relevance of flagellar motility in soil bacterial communities

Ramoneda,

Fan,

Lucas

et al. 2024

Preprint

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Flagellar motility is a key bacterial trait as it allows bacteria to navigate their immediate surroundings. Not all bacteria are capable of flagellar motility, and the distribution of this trait, its ecological associations, and the life history strategies of flagellated taxa remain poorly characterized. We developed and validated a genome-based approach to infer the potential for flagellar motility across 12 bacterial phyla (26,192 genomes in total). The capacity for flagellar motility was associated with a higher prevalence of genes for carbohydrate metabolism and higher maximum potential growth rates, suggesting that flagellar motility is more prevalent in resource-rich environments due to the energetic costs associated with this trait. To test this hypothesis, we focused on soil bacterial communities, where flagellar motility is expected to be particularly important given the heterogeneous nature of the soil environment. We applied a method to infer the prevalence of flagellar motility in whole bacterial communities from metagenomic data, and quantified the prevalence of flagellar motility across 4 independent field studies that each captured putative gradients in soil carbon availability (148 metagenomes). As expected, we observed a positive relationship between the prevalence of bacterial flagellar motility and soil carbon availability in each of these datasets. Given that soil carbon availability is often correlated with other factors that could influence the prevalence of flagellar motility, we validated these observations using metagenomic data acquired from a soil incubation experiment where carbon availability was directly manipulated with glucose amendments, confirming that the prevalence of bacterial flagellar motility is consistently associated with soil carbon availability over other potential confounding factors. Flagellar motility is a fundamental phenotypic trait for bacterial adaptation to soil, defining life history strategies primarily associated with resource availability. More generally, this work highlights the value of combining genomic and metagenomic approaches to expand our understanding of microbial phenotypic traits and reveal their general environmental associations.

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Flagellar Genes Are Associated with the Colonization Persistence Phenotype of the Drosophila melanogaster Microbiota

Cited by 9 publications

References 51 publications

MprF-mediated immune evasion is necessary forLactiplantibacillus plantarumresilience inDrosophilagut during inflammation

MprF-mediated immune evasion is necessary forLactiplantibacillus plantarumresilience inDrosophilagut during inflammation

Massively parallel mutant selection identifies genetic determinants ofPseudomonas aeruginosacolonization ofDrosophila melanogaster

The ecological relevance of flagellar motility in soil bacterial communities

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