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.
三种拟aburkholderia能够与变形虫Dictyostelium disideum形成兼性共生关系。这些共生的副aburkholderia共有一种VI型分泌系统(T6SS),这在其他近亲中是不存在的。本研究检测了松果树tsh atp酶基因断裂对松果树与盘状松果树共生的表型和转录影响。我们假设,∆tssH突变体影响宿主适应性或在宿主间传播的能力将显著降低。我们发现T6SS并不直接影响宿主适应度。相反,与∆tssH相比,野生型白桦具有显著更高的水平传播率。此外,我们观察到,在缺乏环境共生体获取机会的情况下,野生型与∆tssH共生体在多个宿主社会阶段的感染流行范围存在显著差异。成功的共生体传播对维持共生关系有重要贡献。因此,共享的T6SS对于盘状棘球蚴及其副棘球蚴共生体之间的长期进化关系似乎是必要的。在RNA-seq时间序列中,被野生型和∆tssH P. bonniea感染的宿主之间的宿主基因表达模式无法区分,证实了宿主适应度结果没有差异。这些数据也提供了对拟aburkholderia共生体如何逃避其阿米巴宿主的吞噬的见解。最重要的是,细胞氧化剂解毒和溶酶体水解酶的递送似乎受到宿主-共生体串扰的推动和拉动。