Anna Chen, Rachel M Covitz, Abigail A Folsom, Xiangxi Mu, Ronald F Peck, Suegene Noh
{"title":"Symbiotic T6SS affects horizontal transmission of <i>Paraburkholderia bonniea</i> among <i>Dictyostelium discoideum</i> amoeba hosts.","authors":"Anna Chen, Rachel M Covitz, Abigail A Folsom, Xiangxi Mu, Ronald F Peck, Suegene Noh","doi":"10.1093/ismeco/ycaf005","DOIUrl":null,"url":null,"abstract":"<p><p>Three species of <i>Paraburkholderia</i> are able to form facultative symbiotic relationships with the amoeba, <i>Dictyostelium discoideum</i>. These symbiotic <i>Paraburkholderia</i> share a type VI secretion system (T6SS) that is absent in other close relatives. We tested the phenotypic and transcriptional effect of <i>tssH</i> ATPase gene disruption in <i>P. bonniea</i> on its symbiosis with <i>D. discoideum</i>. We hypothesized that the ∆<i>tssH</i> mutant would have a significantly reduced ability to affect host fitness or transmit itself from host to host. We found that the T6SS does not directly affect host fitness. Instead, wildtype <i>P. bonniea</i> had significantly higher rates of horizontal transmission compared to ∆<i>tssH</i>. In addition, we observed significant differences in the range of infection prevalence achieved by wildtype vs. ∆<i>tssH</i> symbionts over multiple host social stages in the absence of opportunities for environmental symbiont acquisition. Successful symbiont transmission significantly contributes to sustained symbiotic association. Therefore, the shared T6SS appears necessary for a long-term evolutionary relationship between <i>D. discoideum</i> and its <i>Paraburkholderia</i> symbionts. The lack of difference in host fitness outcomes was confirmed by indistinguishable host gene expression patterns between hosts infected by wildtype or ∆<i>tssH P. bonniea</i> in an RNA-seq time series. These data also provided insight into how <i>Paraburkholderia</i> symbionts may evade phagocytosis by its amoeba host. Most significantly, cellular oxidant detoxification and lysosomal hydrolase delivery appear to be subject to the push and pull of host-symbiont crosstalk.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf005"},"PeriodicalIF":5.1000,"publicationDate":"2025-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11882306/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"ISME communications","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1093/ismeco/ycaf005","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/1/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"ECOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Three species of Paraburkholderia are able to form facultative symbiotic relationships with the amoeba, Dictyostelium discoideum. These symbiotic Paraburkholderia share a type VI secretion system (T6SS) that is absent in other close relatives. We tested the phenotypic and transcriptional effect of tssH ATPase gene disruption in P. bonniea on its symbiosis with D. discoideum. We hypothesized that the ∆tssH mutant would have a significantly reduced ability to affect host fitness or transmit itself from host to host. We found that the T6SS does not directly affect host fitness. Instead, wildtype P. bonniea had significantly higher rates of horizontal transmission compared to ∆tssH. In addition, we observed significant differences in the range of infection prevalence achieved by wildtype vs. ∆tssH symbionts over multiple host social stages in the absence of opportunities for environmental symbiont acquisition. Successful symbiont transmission significantly contributes to sustained symbiotic association. Therefore, the shared T6SS appears necessary for a long-term evolutionary relationship between D. discoideum and its Paraburkholderia symbionts. The lack of difference in host fitness outcomes was confirmed by indistinguishable host gene expression patterns between hosts infected by wildtype or ∆tssH P. bonniea in an RNA-seq time series. These data also provided insight into how Paraburkholderia symbionts may evade phagocytosis by its amoeba host. Most significantly, cellular oxidant detoxification and lysosomal hydrolase delivery appear to be subject to the push and pull of host-symbiont crosstalk.