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...

Full description

Bibliographic Details
Main Authors: Qiannan Guo, Yuhua Zhan, Wei Zhang, Jin Wang, Yongliang Yan, Wenxiu Wang, Min Lin
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
Description
Summary: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.
ISSN:1661-6596
1422-0067