Cellular adaptation of Clostridioides difficile to high salinity encompasses a compatible solute‐responsive change in cell morphology

Summary Infections by the pathogenic gut bacterium Clostridioides difficile cause severe diarrhoeas up to a toxic megacolon and are currently among the major causes of lethal bacterial infections. Successful bacterial propagation in the gut is strongly associated with the adaptation to changing nutr...

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Published in:	Environmental microbiology Vol. 24; no. 3; pp. 1499 - 1517
Main Authors:	Michel, Annika‐Marisa, Borrero‐de Acuña, José Manuel, Molinari, Gabriella, Ünal, Can Murat, Will, Sabine, Derksen, Elisabeth, Barthels, Stefan, Bartram, Wiebke, Schrader, Michel, Rohde, Manfred, Zhang, Hao, Hoffmann, Tamara, Neumann‐Schaal, Meina, Bremer, Erhard, Jahn, Dieter
Format:	Journal Article
Language:	English
Published:	Hoboken, USA John Wiley & Sons, Inc 01-03-2022 Wiley Subscription Services, Inc
Subjects:	Adaptation Adaptation, Physiological Bacteria Bacterial diseases Bacterial infections Betaine Betaine - metabolism Biocompatibility Carnitine Cell morphology Cells Cellular stress response Chemical synthesis Choline Clostridioides difficile Colon Cytology Energy metabolism Environmental conditions Fermentation Glycine Glycine (amino acid) Growth Infections Metabolism Metabolomics Nutrition Pathogens Proline Proline - metabolism Salinity Salinity effects Salts Sodium chloride Solutes
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Summary:	Summary Infections by the pathogenic gut bacterium Clostridioides difficile cause severe diarrhoeas up to a toxic megacolon and are currently among the major causes of lethal bacterial infections. Successful bacterial propagation in the gut is strongly associated with the adaptation to changing nutrition‐caused environmental conditions; e.g. environmental salt stresses. Concentrations of 350 mM NaCl, the prevailing salinity in the colon, led to significantly reduced growth of C. difficile. Metabolomics of salt‐stressed bacteria revealed a major reduction of the central energy generation pathways, including the Stickland‐fermentation reactions. No obvious synthesis of compatible solutes was observed up to 24 h of growth. The ensuing limited tolerance to high salinity and absence of compatible solute synthesis might result from an evolutionary adaptation to the exclusive life of C. difficile in the mammalian gut. Addition of the compatible solutes carnitine, glycine‐betaine, γ‐butyrobetaine, crotonobetaine, homobetaine, proline‐betaine and dimethylsulfoniopropionate restored growth (choline and proline failed) under conditions of high salinity. A bioinformatically identified OpuF‐type ABC‐transporter imported most of the used compatible solutes. A long‐term adaptation after 48 h included a shift of the Stickland fermentation‐based energy metabolism from the utilization to the accumulation of l‐proline and resulted in restored growth. Surprisingly, salt stress resulted in the formation of coccoid C. difficile cells instead of the typical rod‐shaped cells, a process reverted by the addition of several compatible solutes. Hence, compatible solute import via OpuF is the major immediate adaptation strategy of C. difficile to high salinity‐incurred cellular stress.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23
ISSN:	1462-2912 1462-2920
DOI:	10.1111/1462-2920.15925