Guoxu Ao , Changli Wang , Liguo Yang , Yue Ma , Zhaoxuan Wang , Yueqi Shi , Shanshan Sun , Wenxiang Ping
{"title":"Quorum sensing: the “switch” in the competitive relationship between Gram-positive bacteria based on transcriptomic analysis","authors":"Guoxu Ao , Changli Wang , Liguo Yang , Yue Ma , Zhaoxuan Wang , Yueqi Shi , Shanshan Sun , Wenxiang Ping","doi":"10.1016/j.micres.2024.127961","DOIUrl":null,"url":null,"abstract":"<div><div>Competition phenomenon is widely presented in nature, however, few reports on the competition phenomenon between bacteria based on the perspective of quorum sensing (QS), especially between Gram-positive bacteria. Here, the Gram-positive bacteria <em>Rhodococcus</em> sp. HD1 and <em>Microbacterium</em> sp<em>.</em> HM-2 were co-cultured, and the epiphysiological indicators, transcriptomics combined with gene engineering technique were applied to clarify the role of QS in the competition between Gram-positive bacteria. The results showed that the morphology of strain HD1 was changed into ellipsoids from long rods, the surface-to-volume ratio increased, and the competition index increased within strains HM-2 and HD1. The biomass of strain HD1(8.06×10<sup>7</sup> CFU/mL) was decreased significantly (<em>p</em><0.05) under co-culture system, compared with mono-culture (5.75×10<sup>8</sup> CFU/mL), indicating that strain HM-2 had an inhibitory effect on HD1 at 12 h. Transcriptomic analysis revealed that QS-related genes were highly expressed in strain HM-2, and the expression level of the virulence gene <em>TM_0352</em> was the highest (FPKM: 1774.19). Meanwhile, the ABC transporters-related genes in strain HD1 were significantly increased. Furthermore, QS pathway-related genes in strain HM-2 and ABC transporters-related genes in strain HD1 showed a significant correlation with the gene <em>TM_0352</em> expression by the Mantel test analysis (<em>p</em><0.05), surmising that the <em>TM_0352</em> gene played a dominant role in the co-culture system. Knockout and complementation experiments confirmed that the function of gene <em>TM_0352</em>. The structural equation model showed that the QS up-regulation of strain HM-2 significantly promoted the expression of virulence genes, while strain HD1 promoted ABC transporters to cope with the up-regulation of <em>TM_0352</em>. The up-regulation of <em>TM_0352</em> promoted the biomass of strain HM-2 and inhibited the biomass of HD1.The above results displayed that the competition phenomenon appeared by QS driving the up-regulation of <em>TM_0352</em> gene in strain HM-2, which led to the up-regulation of ABC transporters in strain HD1. And these findings provided new insights into the perspective of factors related to competition inhibition between bacteria.</div></div>","PeriodicalId":18564,"journal":{"name":"Microbiological research","volume":null,"pages":null},"PeriodicalIF":6.1000,"publicationDate":"2024-10-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Microbiological research","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0944501324003628","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Competition phenomenon is widely presented in nature, however, few reports on the competition phenomenon between bacteria based on the perspective of quorum sensing (QS), especially between Gram-positive bacteria. Here, the Gram-positive bacteria Rhodococcus sp. HD1 and Microbacterium sp. HM-2 were co-cultured, and the epiphysiological indicators, transcriptomics combined with gene engineering technique were applied to clarify the role of QS in the competition between Gram-positive bacteria. The results showed that the morphology of strain HD1 was changed into ellipsoids from long rods, the surface-to-volume ratio increased, and the competition index increased within strains HM-2 and HD1. The biomass of strain HD1(8.06×107 CFU/mL) was decreased significantly (p<0.05) under co-culture system, compared with mono-culture (5.75×108 CFU/mL), indicating that strain HM-2 had an inhibitory effect on HD1 at 12 h. Transcriptomic analysis revealed that QS-related genes were highly expressed in strain HM-2, and the expression level of the virulence gene TM_0352 was the highest (FPKM: 1774.19). Meanwhile, the ABC transporters-related genes in strain HD1 were significantly increased. Furthermore, QS pathway-related genes in strain HM-2 and ABC transporters-related genes in strain HD1 showed a significant correlation with the gene TM_0352 expression by the Mantel test analysis (p<0.05), surmising that the TM_0352 gene played a dominant role in the co-culture system. Knockout and complementation experiments confirmed that the function of gene TM_0352. The structural equation model showed that the QS up-regulation of strain HM-2 significantly promoted the expression of virulence genes, while strain HD1 promoted ABC transporters to cope with the up-regulation of TM_0352. The up-regulation of TM_0352 promoted the biomass of strain HM-2 and inhibited the biomass of HD1.The above results displayed that the competition phenomenon appeared by QS driving the up-regulation of TM_0352 gene in strain HM-2, which led to the up-regulation of ABC transporters in strain HD1. And these findings provided new insights into the perspective of factors related to competition inhibition between bacteria.
期刊介绍:
Microbiological Research is devoted to publishing reports on prokaryotic and eukaryotic microorganisms such as yeasts, fungi, bacteria, archaea, and protozoa. Research on interactions between pathogenic microorganisms and their environment or hosts are also covered.