Survival characteristics and transcriptome profiling reveal the adaptive response of the Brucella melitensis 16M biofilm to osmotic stress
Brucella can inhabit hostile environments, including osmotic stress. How Brucella responds collectively to osmotic stress is largely unexplored, particularly in spatially structured communities such as a biofilm. To gain insight into this growth mode, we set out to characterize the Brucella melitens...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-08-01
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| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.968592/full |
| _version_ | 1798037234936446976 |
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| author | Jia Guo Jiale Zhu Tianyi Zhao Zhihua Sun Shengnan Song Yu Zhang Dexin Zhu Shuzhu Cao Xingmei Deng Yingjin Chai Yongxue Sun Suleimenov Maratbek Suleimenov Maratbek Chuangfu Chen Liangbo Liu Hui Zhang |
| author_facet | Jia Guo Jiale Zhu Tianyi Zhao Zhihua Sun Shengnan Song Yu Zhang Dexin Zhu Shuzhu Cao Xingmei Deng Yingjin Chai Yongxue Sun Suleimenov Maratbek Suleimenov Maratbek Chuangfu Chen Liangbo Liu Hui Zhang |
| author_sort | Jia Guo |
| collection | DOAJ |
| description | Brucella can inhabit hostile environments, including osmotic stress. How Brucella responds collectively to osmotic stress is largely unexplored, particularly in spatially structured communities such as a biofilm. To gain insight into this growth mode, we set out to characterize the Brucella melitensis 16M biofilm, describe its phenotype, and carry out a comparative transcriptomic analysis between biofilms under osmotic stress and control conditions. We determined that the bacteria challenged with 1.5 M NaCl had a reduced ability to aggregate and form clumps and develop a biofilm; however, the salt stress promoted the release of the outer membrane vesicles from the biofilm. Together with the genotypical response to osmotic stress, we identified 279 differentially expressed genes in B. melitensis 16M grown under osmotic conditions compared with control conditions; 69 genes were upregulated and 210 downregulated. Under osmotic stress, the main changed genes of biofilm were predicted to be involved in flagellar assembly, cell envelope, translation, small RNA regulation, transport and binding proteins, and energy metabolism. In addition, the ABC transporter was enriched in the Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways. We highlight 12 essential ABC transporter genes associated with a bacterial response to osmotic stress at the biofilm stage, including one specific locus, BME_RS12880, mediating betaine accumulation in biofilms to eliminate osmotic stress. The current study results can help researchers gain insights into B. melitensis 16M biofilm adaptation to osmotic stress and provide information for developing intervention strategies to control Brucella. |
| first_indexed | 2024-04-11T21:23:50Z |
| format | Article |
| id | doaj.art-50a7e71b43f349dd8995d85b44106188 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-11T21:23:50Z |
| publishDate | 2022-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-50a7e71b43f349dd8995d85b441061882022-12-22T04:02:29ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-08-011310.3389/fmicb.2022.968592968592Survival characteristics and transcriptome profiling reveal the adaptive response of the Brucella melitensis 16M biofilm to osmotic stressJia Guo0Jiale Zhu1Tianyi Zhao2Zhihua Sun3Shengnan Song4Yu Zhang5Dexin Zhu6Shuzhu Cao7Xingmei Deng8Yingjin Chai9Yongxue Sun10Suleimenov Maratbek11Suleimenov Maratbek12Chuangfu Chen13Liangbo Liu14Hui Zhang15State International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi, ChinaCollaborative Innovation Center for Sheep Healthy Farming and Zoonotic Disease Control, College of Veterinary Medicine, South China Agricultural University, Guangzhou, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi, ChinaCollege of Veterinary, National Agricultural University of Kazakhstan, Nur-Sultan, KazakhstanState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi, ChinaState International Joint Research Center for Animal Health Breeding, College of Animal Science and Technology, Shihezi University, Shihezi, ChinaBrucella can inhabit hostile environments, including osmotic stress. How Brucella responds collectively to osmotic stress is largely unexplored, particularly in spatially structured communities such as a biofilm. To gain insight into this growth mode, we set out to characterize the Brucella melitensis 16M biofilm, describe its phenotype, and carry out a comparative transcriptomic analysis between biofilms under osmotic stress and control conditions. We determined that the bacteria challenged with 1.5 M NaCl had a reduced ability to aggregate and form clumps and develop a biofilm; however, the salt stress promoted the release of the outer membrane vesicles from the biofilm. Together with the genotypical response to osmotic stress, we identified 279 differentially expressed genes in B. melitensis 16M grown under osmotic conditions compared with control conditions; 69 genes were upregulated and 210 downregulated. Under osmotic stress, the main changed genes of biofilm were predicted to be involved in flagellar assembly, cell envelope, translation, small RNA regulation, transport and binding proteins, and energy metabolism. In addition, the ABC transporter was enriched in the Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways. We highlight 12 essential ABC transporter genes associated with a bacterial response to osmotic stress at the biofilm stage, including one specific locus, BME_RS12880, mediating betaine accumulation in biofilms to eliminate osmotic stress. The current study results can help researchers gain insights into B. melitensis 16M biofilm adaptation to osmotic stress and provide information for developing intervention strategies to control Brucella.https://www.frontiersin.org/articles/10.3389/fmicb.2022.968592/fulltranscriptomeBrucella melitensis 16MABC transporterbetainebiofilmosmotic stress |
| spellingShingle | Jia Guo Jiale Zhu Tianyi Zhao Zhihua Sun Shengnan Song Yu Zhang Dexin Zhu Shuzhu Cao Xingmei Deng Yingjin Chai Yongxue Sun Suleimenov Maratbek Suleimenov Maratbek Chuangfu Chen Liangbo Liu Hui Zhang Survival characteristics and transcriptome profiling reveal the adaptive response of the Brucella melitensis 16M biofilm to osmotic stress Frontiers in Microbiology transcriptome Brucella melitensis 16M ABC transporter betaine biofilm osmotic stress |
| title | Survival characteristics and transcriptome profiling reveal the adaptive response of the Brucella melitensis 16M biofilm to osmotic stress |
| title_full | Survival characteristics and transcriptome profiling reveal the adaptive response of the Brucella melitensis 16M biofilm to osmotic stress |
| title_fullStr | Survival characteristics and transcriptome profiling reveal the adaptive response of the Brucella melitensis 16M biofilm to osmotic stress |
| title_full_unstemmed | Survival characteristics and transcriptome profiling reveal the adaptive response of the Brucella melitensis 16M biofilm to osmotic stress |
| title_short | Survival characteristics and transcriptome profiling reveal the adaptive response of the Brucella melitensis 16M biofilm to osmotic stress |
| title_sort | survival characteristics and transcriptome profiling reveal the adaptive response of the brucella melitensis 16m biofilm to osmotic stress |
| topic | transcriptome Brucella melitensis 16M ABC transporter betaine biofilm osmotic stress |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.968592/full |
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