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C-Di-AMP Signaling Is Required for Bile Salts Resistance and Long-Term

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C-Di-AMP Signaling Is Required for Bile Salts Resistance and Long-Term bioRxiv preprint doi: https://doi.org/10.1101/2021.08.23.457418; this version posted August 23, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Title: c-di-AMP signaling is required for bile salts resistance and long-term 2 colonization by Clostridioides difficile 3 Authors: Marine Oberkampf1†, Audrey Hamiot1‡†, Pamela Altamirano-Silva2, Paula Bellés- 4 Sancho1§, Yannick D. N. Tremblay1¶, Nicholas DiBenedetto3, Roland Seifert4, Olga 5 Soutourina5, Lynn Bry3,6, Bruno Dupuy1* and Johann Peltier1,5* 6 7 Affiliations: 8 1. Laboratoire Pathogenèse des Bactéries Anaérobies, CNRS-2001, Institut Pasteur, 9 Université de Paris, F-75015 Paris, France. 10 2. Centro de Investigación en Enfermedades Tropicales, Facultad de Microbiología, 11 Universidad de Costa Rica, San José, Costa Rica 12 3. Massachusetts Host-Microbiome Center, Dept. Pathology, Brigham & Women’s Hospital, 13 Harvard Medical School, Boston, MA. 14 4. Institute of Pharmacology & Research Core Unit Metabolomics, Hannover Medical 15 School, Hannover, Germany. 16 5. Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 17 91198, Gif-sur-Yvette, France 18 6. Clinical Microbiology Laboratory, Department of Pathology, Brigham & Women’s 19 Hospital, Boston, MA. 20 21 * Co-corresponding authors. Emails: [email protected]; [email protected] 22 saclay.fr 23 24 † These authors contributed equally to the studies undertaken. 25 ‡ Present address: UMR UMET, INRA, CNRS, Univ. Lille 1, 59650 Villeneuve d'Ascq, 26 France. 27 § Present address: Department of Plant and Microbial Biology, University of Zürich, CH-8057 28 Zürich, Switzerland. 29 ¶ Present address: Department of Biochemistry, Microbiology and Immunology, University of 30 Saskatchewan, Saskatoon, Canada. 31 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.23.457418; this version posted August 23, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 32 ABSTRACT 33 To cause disease, the important human enteropathogen Clostridioides difficile must colonize 34 the gastro-intestinal tract but little is known on how this organism senses and responds to the 35 harsh host environment to adapt and multiply. Nucleotide second messengers are signaling 36 molecules used by bacteria to respond to changing environmental conditions. In this study, we 37 showed for the first time that c-di-AMP is produced by C. difficile and controls the uptake of 38 potassium, making it essential for growth. We found that c-di-AMP is involved in biofilm 39 formation, cell wall homeostasis, osmotolerance as well as detergent and bile salt resistance in 40 C. difficile. In a colonization mouse model, a strain lacking GdpP, a c-di-AMP degrading 41 enzyme, failed to persist in the gut in contrast to the parental strain. We identified OpuR as a 42 new regulator that binds c-di-AMP and represses the expression of the compatible solute 43 transporter OpuC. Interestingly, an opuR mutant is highly resistant to a hyperosmotic or bile 44 salt stress compared to the parental strain while an opuCA mutant is more susceptible A short 45 exposure of C. difficile cells to bile salts resulted in a decrease of the c-di-AMP concentrations 46 reinforcing the hypothesis that changes in membrane characteristics due to variations of the 47 cellular turgor or membrane damages constitute a signal for the adjustment of the intracellular 48 c-di-AMP concentration. Thus, c-di-AMP is a signaling molecule with pleiotropic effects that 49 controls osmolyte uptake to confer osmotolerance and bile salt resistance in C. difficile and that 50 is important for colonization of the host. 51 52 One Sentence Summary: c-di-AMP is an essential regulatory molecule conferring resistance 53 to osmotic and bile salt stresses by controlling osmolyte uptake and contributing to gut 54 persistence in the human enteropathogen Clostridioides difficile. 55 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.23.457418; this version posted August 23, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 56 INTRODUCTION 57 Clostridioides difficile is a medically important human enteropathogen that became a public 58 health concern over the last two decades in industrialized countries (1, 2). This strict anaerobic 59 spore-forming Gram-positive bacterium is a major cause of antibiotic-associated nosocomial 60 diarrhoea in adults (3). Most virulent C. difficile strains produce two glycosylating toxins 61 (TcdA and TcdB) which play a key role in disease pathogenesis by targeting the gut epithelium 62 resulting in severe inflammation and damage to the colon (4, 5). Transmission of C. difficile is 63 dependent on the production of highly resistant spores, which germinate in the small intestine 64 in response to primary bile salts (6, 7). Normally the intestinal microbiota mediates 65 colonization resistance against C. difficile but an antibiotic treatment disrupts the host 66 microbiota, resulting in C. difficile growth, colonization of the intestine and toxin production 67 (8, 9). 68 During the course of infection along the gastrointestinal tract of the host, C. difficile encounters 69 multiple stresses, including numerous antimicrobial compounds, abrupt shifts in pH, reactive 70 oxygen species produced during inflammation and the host immune response to infection (10- 71 12). C. difficile vegetative cells are also exposed to primary and secondary bile salts. Primary 72 bile salts produced by the human liver consists mainly s of cholate and chenodeoxycholate 73 conjugated with either taurine or glycine. Secondary bile salts, predominantly comprising of 74 deoxycholate and lithocholate in humans, are derived from primary bile salts by modifications 75 carried out by intestinal bacteria (13). While the primary bile salt taurocholate induces spore 76 germination, the secondary bile salt deoxycholate is a poor germinant and inhibits vegetative 77 cell growth (14). Another important stress in the intestinal lumen is the high osmolarity 78 (equivalent to 300 mM sodium chloride (NaCl)) (15). 79 Bacteria respond to osmotic stresses by adjusting their intracellular concentrations of 80 osmolytes to limit transmembrane water fluxes and maintain turgor. The emergency response bioRxiv preprint doi: https://doi.org/10.1101/2021.08.23.457418; this version posted August 23, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 81 against an hyperosmotic shock is the uptake of potassium (K+) and it is followed by the 82 synthesis and/or import of compatible solutes, such as carnitine and glycine betaine that act as 83 osmoprotectants (16). These generally neutral compounds are preferred osmolytes because 84 they can accumulate to very high concentrations without inducing severe disturbances in 85 cellular metabolism (17). Several osmolyte transport systems have been identified in Gram- 86 positive bacteria and interestingly, many of these transporters are controlled by the second 87 messenger cyclic diadenosine monophosphate (c-di-AMP) (18). As an example, c-di-AMP 88 inhibits the three K+ transport systems in Bacillus subtilis (the high affinities KimA and KtrAB 89 and the low affinity KtrCD transport systems) (19), negatively controls the activity of the OpuC 90 carnitine transporter in Listeria monocytogenes and Staphylococcus aureus or binds to the 91 BusR repressor controlling the expression of the glycine betaine transporter genes busAA- 92 busAB in Lactococcus lactis and Streptococcus agalactiae (20, 21). 93 C-di-AMP is widely produced among Gram-positive bacteria with many c-di-AMP 94 synthesizing organisms being prominent human pathogens. C-di-AMP is synthesized from two 95 molecules of ATP by di-adenylate cyclase (DAC) enzymes and degraded to pApA or AMP by 96 distinct c-di-AMP phosphodiesterase (PDE) enzymes. Most important human pathogens 97 possess only a single DAC domain containing protein called CdaA, which is essential for 98 production of c-di-AMP. However, spore-forming Clostridia and Bacilli contain one (DisA) or 99 two additional DACs (DisA and CdaS), respectively (22) . DisA plays a role in the control of 100 DNA integrity and CdaS is specifically involved in sporulation-related processes (23-26). Two 101 other DACs CdaM and CdaZ are present only in few organisms (27, 28). Four different classes 102 of PDEs degrade c-di-AMP but most of the reported PDEs belong to the membrane-bound 103 GdpP protein family, which consists of a signal regulatory module linked to a GGDEF domain 104 and a DHH-DHHA1 catalytic domain (29) (30, 31) (32). C-di-AMP is essential for growth 105 under standard laboratory conditions in most of the Firmicutes (18, 20, 33-36). However, recent bioRxiv preprint doi: https://doi.org/10.1101/2021.08.23.457418; this version posted August 23, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 106 studies revealed that c-di-AMP becomes dispensable, if the bacteria are cultivated on specific 107 minimal media (19, 20, 35). Moreover, intracellular accumulation of c-di-AMP is also toxic 108 and inhibits growth (37).
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