Development and Regulation of the Extreme Biofilm Formation of <i>Deinococcus radiodurans</i> R1 under Extreme Environmental Conditions
To grow in various harsh environments, extremophiles have developed extraordinary strategies such as biofilm formation, which is an extremely complex and progressive process. However, the genetic elements and exact mechanisms underlying extreme biofilm formation remain enigmatic. Here, we characteri...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2023-12-01
|
| Series: | International Journal of Molecular Sciences |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1422-0067/25/1/421 |
| _version_ | 1797358674141773824 |
|---|---|
| author | Qiannan Guo Yuhua Zhan Wei Zhang Jin Wang Yongliang Yan Wenxiu Wang Min Lin |
| author_facet | Qiannan Guo Yuhua Zhan Wei Zhang Jin Wang Yongliang Yan Wenxiu Wang Min Lin |
| author_sort | Qiannan Guo |
| collection | DOAJ |
| description | To grow in various harsh environments, extremophiles have developed extraordinary strategies such as biofilm formation, which is an extremely complex and progressive process. However, the genetic elements and exact mechanisms underlying extreme biofilm formation remain enigmatic. Here, we characterized the biofilm-forming ability of <i>Deinococcus radiodurans</i> in vitro under extreme environmental conditions and found that extremely high concentrations of NaCl or sorbitol could induce biofilm formation. Meantime, the survival ability of biofilm cells was superior to that of planktonic cells in different extreme conditions, such as hydrogen peroxide stress, sorbitol stress, and high UV radiation. Transcriptome profiles of <i>D. radiodurans</i> in four different biofilm development stages further revealed that only 13 matched genes, which are involved in environmental information processing, carbohydrate metabolism, or stress responses, share sequence homology with genes related to the biofilm formation of <i>Escherichia coli</i>, <i>Pseudomonas aeruginosa</i>, and <i>Staphylococcus aureus</i>. Overall, 64% of the differentially expressed genes are functionally unknown, indicating the specificity of the regulatory network of <i>D. radiodurans</i>. The mutation of the <i>drRRA</i> gene encoding a response regulator strongly impaired biofilm formation ability, implying that DrRRA is an essential component of the biofilm formation of <i>D. radiodurans</i>. Furthermore, transcripts from both the wild type and the <i>drRRA</i> mutant were compared, showing that the expression of <i>drBON1</i> (<i>Deinococcus radiodurans</i>BON domain-containing protein 1) significantly decreased in the <i>drRRA</i> mutant during biofilm development. Further analysis revealed that the <i>drBON1</i> mutant lacked the ability to form biofilm and DrRRA, and as a facilitator of biofilm formation, could directly stimulate the transcription of the biofilm-related gene <i>drBON1</i>. Overall, our work highlights a molecular mechanism mediated by the response regulator DrRRA for controlling extreme biofilm formation and thus provides guidance for future studies to investigate novel mechanisms that are used by <i>D. radiodurans</i> to adapt to extreme environments. |
| first_indexed | 2024-03-08T15:05:28Z |
| format | Article |
| id | doaj.art-8d02f82fdd094561900b8a163bb5329b |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-08T15:05:28Z |
| publishDate | 2023-12-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-8d02f82fdd094561900b8a163bb5329b2024-01-10T14:59:26ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-12-0125142110.3390/ijms25010421Development and Regulation of the Extreme Biofilm Formation of <i>Deinococcus radiodurans</i> R1 under Extreme Environmental ConditionsQiannan Guo0Yuhua Zhan1Wei Zhang2Jin Wang3Yongliang Yan4Wenxiu Wang5Min Lin6National Key Laboratory of Agricultural Microbiology, Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaNational Key Laboratory of Agricultural Microbiology, Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaNational Key Laboratory of Agricultural Microbiology, Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaNational Key Laboratory of Agricultural Microbiology, Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaNational Key Laboratory of Agricultural Microbiology, Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaNational Key Laboratory of Agricultural Microbiology, Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaNational Key Laboratory of Agricultural Microbiology, Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaTo grow in various harsh environments, extremophiles have developed extraordinary strategies such as biofilm formation, which is an extremely complex and progressive process. However, the genetic elements and exact mechanisms underlying extreme biofilm formation remain enigmatic. Here, we characterized the biofilm-forming ability of <i>Deinococcus radiodurans</i> in vitro under extreme environmental conditions and found that extremely high concentrations of NaCl or sorbitol could induce biofilm formation. Meantime, the survival ability of biofilm cells was superior to that of planktonic cells in different extreme conditions, such as hydrogen peroxide stress, sorbitol stress, and high UV radiation. Transcriptome profiles of <i>D. radiodurans</i> in four different biofilm development stages further revealed that only 13 matched genes, which are involved in environmental information processing, carbohydrate metabolism, or stress responses, share sequence homology with genes related to the biofilm formation of <i>Escherichia coli</i>, <i>Pseudomonas aeruginosa</i>, and <i>Staphylococcus aureus</i>. Overall, 64% of the differentially expressed genes are functionally unknown, indicating the specificity of the regulatory network of <i>D. radiodurans</i>. The mutation of the <i>drRRA</i> gene encoding a response regulator strongly impaired biofilm formation ability, implying that DrRRA is an essential component of the biofilm formation of <i>D. radiodurans</i>. Furthermore, transcripts from both the wild type and the <i>drRRA</i> mutant were compared, showing that the expression of <i>drBON1</i> (<i>Deinococcus radiodurans</i>BON domain-containing protein 1) significantly decreased in the <i>drRRA</i> mutant during biofilm development. Further analysis revealed that the <i>drBON1</i> mutant lacked the ability to form biofilm and DrRRA, and as a facilitator of biofilm formation, could directly stimulate the transcription of the biofilm-related gene <i>drBON1</i>. Overall, our work highlights a molecular mechanism mediated by the response regulator DrRRA for controlling extreme biofilm formation and thus provides guidance for future studies to investigate novel mechanisms that are used by <i>D. radiodurans</i> to adapt to extreme environments.https://www.mdpi.com/1422-0067/25/1/421extreme environment<i>Deinococcus radiodurans</i>biofilm formationtranscriptome profileresponse regulator DrRRA |
| spellingShingle | Qiannan Guo Yuhua Zhan Wei Zhang Jin Wang Yongliang Yan Wenxiu Wang Min Lin Development and Regulation of the Extreme Biofilm Formation of <i>Deinococcus radiodurans</i> R1 under Extreme Environmental Conditions International Journal of Molecular Sciences extreme environment <i>Deinococcus radiodurans</i> biofilm formation transcriptome profile response regulator DrRRA |
| title | Development and Regulation of the Extreme Biofilm Formation of <i>Deinococcus radiodurans</i> R1 under Extreme Environmental Conditions |
| title_full | Development and Regulation of the Extreme Biofilm Formation of <i>Deinococcus radiodurans</i> R1 under Extreme Environmental Conditions |
| title_fullStr | Development and Regulation of the Extreme Biofilm Formation of <i>Deinococcus radiodurans</i> R1 under Extreme Environmental Conditions |
| title_full_unstemmed | Development and Regulation of the Extreme Biofilm Formation of <i>Deinococcus radiodurans</i> R1 under Extreme Environmental Conditions |
| title_short | Development and Regulation of the Extreme Biofilm Formation of <i>Deinococcus radiodurans</i> R1 under Extreme Environmental Conditions |
| title_sort | development and regulation of the extreme biofilm formation of i deinococcus radiodurans i r1 under extreme environmental conditions |
| topic | extreme environment <i>Deinococcus radiodurans</i> biofilm formation transcriptome profile response regulator DrRRA |
| url | https://www.mdpi.com/1422-0067/25/1/421 |
| work_keys_str_mv | AT qiannanguo developmentandregulationoftheextremebiofilmformationofideinococcusradioduransir1underextremeenvironmentalconditions AT yuhuazhan developmentandregulationoftheextremebiofilmformationofideinococcusradioduransir1underextremeenvironmentalconditions AT weizhang developmentandregulationoftheextremebiofilmformationofideinococcusradioduransir1underextremeenvironmentalconditions AT jinwang developmentandregulationoftheextremebiofilmformationofideinococcusradioduransir1underextremeenvironmentalconditions AT yongliangyan developmentandregulationoftheextremebiofilmformationofideinococcusradioduransir1underextremeenvironmentalconditions AT wenxiuwang developmentandregulationoftheextremebiofilmformationofideinococcusradioduransir1underextremeenvironmentalconditions AT minlin developmentandregulationoftheextremebiofilmformationofideinococcusradioduransir1underextremeenvironmentalconditions |