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Published in: Gut Pathogens 1/2023

Open Access 01-12-2023 | Respiratory Microbiota | Research

Invasion of intestinal cells by Staphylococcus warneri, a member of the human gut microbiota

Authors: Robin Louail, Franklin Florin, Sophie Bernard, Jean-Baptiste Michaud, Jonathan Breton, Najate Achamrah, Marie-Pierre Tavolacci, Moïse Coëffier, David Ribet

Published in: Gut Pathogens | Issue 1/2023

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Abstract

Coagulase negative staphylococci (CoNS) are a heterogeneous group of bacteria that colonize different types of human epithelia. These bacteria have a highly variable pathogenic potential ranging from avirulent species to major nosocomial pathogens. Staphylococcus warneri is a CoNS species considered to be nonpathogenic. Here, we identify that S. warneri is a natural member of both human and mouse gut microbiota. In addition, we demonstrate that this bacterium is able to get internalized into human cells. We show that S. warneri efficiently invades several human cell types and, more specifically, intestinal epithelial cells, using actin-dependent mechanisms. In contrast to bona fide pathogens, S. warneri does not actively replicate within intestinal cells or resist killing by macrophages. Together, our results highlight that bacteria from the human gut microbiota that are not associated with a high pathogenic potential, can actively invade intestinal cells and may, in this way, impact intestinal physiology.

Literature
  1. Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016;14(8): e1002533.View Article
  2. Ribet D, Cossart P. How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect. 2015;17(3):173–83.View Article
  3. Doran KS, Banerjee A, Disson O, Lecuit M. Concepts and mechanisms: crossing host barriers. Cold Spring Harb Perspect Med. 2013;3(7):a010090.View Article
  4. Casadevall A. The pathogenic potential of a microbe. mSphere. 2017;2(1):e00015.View Article
  5. Jochum L, Stecher B. Label or concept—what is a pathobiont? Trends Microbiol. 2020;28(10):789–92.View Article
  6. Becker K, Heilmann C, Peters G. Coagulase-negative staphylococci. Clin Microbiol Rev. 2014;27(4):870–926.View Article
  7. Luqman A, Nega M, Nguyen MT, Ebner P, Gotz F. SadA-expressing Staphylococci in the human gut show increased cell adherence and internalization. Cell Rep. 2018;22(2):535–45.View Article
  8. Khalil H, Williams RJ, Stenbeck G, Henderson B, Meghji S, Nair SP. Invasion of bone cells by Staphylococcus epidermidis. Microbes Infect. 2007;9(4):460–5.View Article
  9. Hirschhausen N, Schlesier T, Schmidt MA, Gotz F, Peters G, Heilmann C. A novel staphylococcal internalization mechanism involves the major autolysin Atl and heat shock cognate protein Hsc70 as host cell receptor. Cell Microbiol. 2010;12(12):1746–64.View Article
  10. Valour F, Trouillet-Assant S, Rasigade JP, Lustig S, Chanard E, Meugnier H, et al. Staphylococcus epidermidis in orthopedic device infections: the role of bacterial internalization in human osteoblasts and biofilm formation. PLoS ONE. 2013;8(6): e67240.View Article
  11. Campoccia D, Montanaro L, Ravaioli S, Cangini I, Testoni F, Visai L, et al. New parameters to quantitatively express the invasiveness of bacterial strains from implant-related orthopaedic infections into osteoblast cells. Materials. 2018;11(4):550.View Article
  12. Savey A, Fleurette J, Salle BL. An analysis of the microbial flora of premature neonates. J Hosp Infect. 1992;21(4):275–89.View Article
  13. Dominguez E, Zarazaga M, Torres C. Antibiotic resistance in Staphylococcus isolates obtained from fecal samples of healthy children. J Clin Microbiol. 2002;40(7):2638–41.View Article
  14. Sanchez E, Ribes-Koninckx C, Calabuig M, Sanz Y. Intestinal Staphylococcus spp. and virulent features associated with coeliac disease. J Clin Pathol. 2012;65(9):830–4.View Article
  15. Hira V, Kornelisse RF, Sluijter M, Kamerbeek A, Goessens WH, de Groot R, et al. Colonization dynamics of antibiotic-resistant coagulase-negative Staphylococci in neonates. J Clin Microbiol. 2013;51(2):595–7.View Article
  16. Aujoulat F, Roudiere L, Picaud JC, Jacquot A, Filleron A, Neveu D, et al. Temporal dynamics of the very premature infant gut dominant microbiota. BMC Microbiol. 2014;14:325.View Article
  17. Golinska E, Strus M, Tomusiak-Plebanek A, Wiecek G, Kozien L, Lauterbach R, et al. Coagulase-negative Staphylococci contained in gut microbiota as a primary source of sepsis in low- and very low birth weight neonates. J Clin Med. 2020;9(8):2517.View Article
  18. Poyart C, Quesne G, Boumaila C, Trieu-Cuot P. Rapid and accurate species-level identification of coagulase-negative staphylococci by using the sodA gene as a target. J Clin Microbiol. 2001;39(12):4296–301.View Article
  19. Elsinghorst EA. Measurement of invasion by gentamicin resistance. Methods Enzymol. 1994;236:405–20.View Article
  20. Isberg RR, Voorhis DL, Falkow S. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell. 1987;50(5):769–78.View Article
  21. Bianchi F, van den Bogaart G. Vacuolar escape of foodborne bacterial pathogens. J Cell Sci. 2020;134(5):jcs247221.View Article
  22. Kloos WE, Schleifer KH. Isolation and Characterization of Staphylococci from Human Skin II. Descriptions of Four New Species: Staphylococcus warneri, Staphylococcus capitis, Staphylococcus hominis, and Staphylococcus simulans. Int J Syst Bacteriol. 1975;25:62–79.View Article
  23. Foster TJ, Geoghegan JA, Ganesh VK, Hook M. Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol. 2014;12(1):49–62.View Article
  24. Carabeo R. Bacterial subversion of host actin dynamics at the plasma membrane. Cell Microbiol. 2011;13(10):1460–9.View Article
  25. Wiedemann A, Linder S, Grassl G, Albert M, Autenrieth I, Aepfelbacher M. Yersinia enterocolitica invasin triggers phagocytosis via beta1 integrins, CDC42Hs and WASp in macrophages. Cell Microbiol. 2001;3(10):693–702.View Article
  26. Lawley TD, Clare S, Walker AW, Stares MD, Connor TR, Raisen C, et al. Targeted restoration of the intestinal microbiota with a simple, defined bacteriotherapy resolves relapsing Clostridium difficile disease in mice. PLoS Pathog. 2012;8(10): e1002995.View Article
  27. Liu C, Zhou N, Du MX, Sun YT, Wang K, Wang YJ, et al. The mouse gut microbial Biobank expands the coverage of cultured bacteria. Nat Commun. 2020;11(1):79.View Article
  28. Kmet V, Cuvalova A, Stanko M. Small mammals as sentinels of antimicrobial-resistant staphylococci. Folia Microbiol. 2018;63(5):665–8.View Article
  29. Bino E, Laukova A, Scerbova J, Kubasova I, Kandricakova A, Strompfova V, et al. Fecal coagulase-negative staphylococci from horses, their species variability, and biofilm formation. Folia Microbiol. 2019;64(6):719–26.View Article
  30. Laukova A, Bino E, Kubasova I, Strompfova V, Miltko R, Belzecki G, et al. Characterisation of faecal Staphylococci from Roe Deer (Capreolus capreolus) and Red Deer (Cervus elaphus) and their susceptibility to Gallidermin. Probiotics Antimicrob Proteins. 2020;12(1):302–10.View Article
  31. Josse J, Laurent F, Diot A. Staphylococcal adhesion and host cell invasion: fibronectin-binding and other mechanisms. Front Microbiol. 2017;8:2433.View Article
  32. Pereira EM, Teixeira CAA, Alvarenga ALM, Schuenck RP, Giambiagi-deMarval M, Holandino C, et al. A Brazilian lineage of Staphylococcus lugdunensis presenting rough colony morphology may adhere to and invade lung epithelial cells. J Med Microbiol. 2012;61(Pt 4):463–9.View Article
  33. Hussain M, Steinbacher T, Peters G, Heilmann C, Becker K. The adhesive properties of the Staphylococcus lugdunensis multifunctional autolysin AtlL and its role in biofilm formation and internalization. Int J Med Microbiol. 2015;305(1):129–39.View Article
  34. Szabados F, Kleine B, Anders A, Kaase M, Sakinc T, Schmitz I, et al. Staphylococcus saprophyticus ATCC 15305 is internalized into human urinary bladder carcinoma cell line 5637. FEMS Microbiol Lett. 2008;285(2):163–9.View Article
  35. Szabados F, Albrecht A, Kleine B, Kaase M, Gatermann S. In contrast to human isolates animal isolates of S. saprophyticus subsp. saprophyticus are not internalized into human urinary bladder carcinoma cell line 5637. Vet Microbiol. 2009;139(3–4):417–8.View Article
  36. Maali Y, Martins-Simoes P, Valour F, Bouvard D, Rasigade JP, Bes M, et al. Pathophysiological mechanisms of Staphylococcus non-aureus bone and joint infection: interspecies homogeneity and specific behavior of S. pseudintermedius. Front Microbiol. 2016;7:1063.View Article
  37. Maali Y, Diot A, Martins-Simoes P, Bes M, Bouvard D, Vandenesch F, et al. Identification and characterization of Staphylococcus delphini internalization pathway in nonprofessional phagocytic cells. Infect Immun. 2020;88(5):e00002.View Article
  38. Soeorg H, Huik K, Parm U, Ilmoja ML, Metelskaja N, Metsvaht T, et al. Genetic relatedness of coagulase-negative Staphylococci from gastrointestinal tract and blood of preterm neonates with late-onset sepsis. Pediatr Infect Dis J. 2013;32(4):389–93.View Article
  39. Tamburini FB, Andermann TM, Tkachenko E, Senchyna F, Banaei N, Bhatt AS. Precision identification of diverse bloodstream pathogens in the gut microbiome. Nat Med. 2018;24(12):1809–14.View Article
  40. Tirelle P, Breton J, Riou G, Dechelotte P, Coeffier M, Ribet D. Comparison of different modes of antibiotic delivery on gut microbiota depletion efficiency and body composition in mouse. BMC Microbiol. 2020;20(1):340.View Article
  41. Fierer N, Jackson JA, Vilgalys R, Jackson RB. Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol. 2005;71(7):4117–20.View Article
Metadata
Title
Invasion of intestinal cells by Staphylococcus warneri, a member of the human gut microbiota
Authors
Robin Louail
Franklin Florin
Sophie Bernard
Jean-Baptiste Michaud
Jonathan Breton
Najate Achamrah
Marie-Pierre Tavolacci
Moïse Coëffier
David Ribet
Publication date
01-12-2023
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2023
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-022-00528-7

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