Inactivation of the SecA2 protein export pathway in Listeria monocytogenes promotes cell aggregation, impacts biofilm architecture and induces biofilm formation in environmental condition

Environmental Microbiology

Volumn 16, Issue 4, 2014, Pages 1176-1192

  Renier, Sandra ^a   Chagnot, Caroline ^a   Deschamps, Julien ^b   Caccia, Nelly ^a   Szlavik, Julie ^c   Joyce, Susan A ^d   Popowska, Magdalena ^e   Hill, Colin ^d   Knøchel, Susanne ^c   Briandet, Romain ^b   Hébraud, Michel ^a   Desvaux, Mickaël ^a  

^a CEMAGREF   (France)

^b UMR1319 MICALIS   (France)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITY COLLEGE CORK   (Ireland)

^e UNIVERSITY OF WARSAW   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

LISTERIA MONOCYTOGENES;

BACTERIAL PROTEIN;

ARTICLE; BIOFILM; CELL AGGREGATION; CONFOCAL MICROSCOPY; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; LISTERIA MONOCYTOGENES; PHYSIOLOGY; TEMPERATURE;

BACTERIAL PROTEINS; BIOFILMS; CELL AGGREGATION; LISTERIA MONOCYTOGENES; MICROSCOPY, CONFOCAL; TEMPERATURE;

EID: 84898058560     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12257     Document Type: Article

References (74)

1. Arnaud, M., Chastanet, A., and Debarbouille, M. (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, Gram-positive bacteria. Appl Environ Microbiol 70: 6887-6891.
2. Bereksi, N., Gavini, F., Benezech, T., and Faille, C. (2002) Growth, morphology and surface properties of Listeria monocytogenes Scott A and LO28 under saline and acid environments. J Appl Microbiol 92: 556-565.
3. Borucki, M.K., Peppin, J.D., White, D., Loge, F., and Call, D.R. (2003) Variation in biofilm formation among strains of Listeria monocytogenes. Appl Environ Microbiol 69: 7336-7342.
4. Brzin, B. (1975) Further observations of changed growth of Listeria monocytogenes on salt agar. Zentralbl Bakteriol [Orig A] 232: 287-293.
5. Carpentier, B., and Cerf, O. (2011) Review - Persistence of Listeria monocytogenes in food industry equipment and premises. Int J Food Microbiol 145: 1-8.
6. Carroll, S.A., Hain, T., Technow, U., Darji, A., Pashalidis, P., Joseph, S.W., and Chakraborty, T. (2003) Identification and characterization of a peptidoglycan hydrolase, MurA, of Listeria monocytogenes, a muramidase needed for cell separation. J Bacteriol 185: 6801-6808.
7. Chae, M.S., and Schraft, H. (2000) Comparative evaluation of adhesion and biofilm formation of different Listeria monocytogenes strains. Int J Food Microbiol 62: 103-111.
8. Chagnot, C., Agus, A., Renier, S., Peyrin, F., Talon, R., Astruc, T., and Desvaux, M. (2013) In vitro colonization of the muscle extracellular matrix components by Escherichia coli O157:H7: the influence of growth medium, temperature and pH on initial adhesion and induction of biofilm formation by collagens I and III. PLoS ONE 8: e59386.
9. Chavant, P., Martinie, B., Meylheuc, T., Bellon-Fontaine, M.N., and Hébraud, M. (2002) Listeria monocytogenes LO28: surface physicochemical properties and ability to form biofilms at different temperatures and growth phases. Appl Environ Microbiol 68: 728-737.
10. Chavant, P., Gaillard-Martinie, B., Talon, R., Hebraud, M., and Bernardi, T. (2007) A new device for rapid evaluation of biofilm formation potential by bacteria. J Microbiol Methods 68: 605-612.
11. Colvin, K.M., Irie, Y., Tart, C.S., Urbano, R., Whitney, J.C., Ryder, C., etal. (2012) The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix. Environ Microbiol 14: 1913-1928.
12. Desvaux, M. (2012) Contribution of holins to protein trafficking: secretion, leakage or lysis? Trends Microbiol 20: 259-261.
13. Desvaux, M., and Hébraud, M. (2006) The protein secretion systems in Listeria: inside out bacterial virulence. FEMS Microbiol Rev 30: 774-805.
14. Desvaux, M., Khan, A., Beatson, S.A., Scott-Tucker, A., and Henderson, I.R. (2005a) Protein secretion systems in Fusobacterium nucleatum: genomic identification of Type 4 piliation and complete Type V pathways brings new insight into mechanisms of pathogenesis. Biochim Biophys Acta-Biomembr 1713: 92-112.
15. Desvaux, M., Khan, A., Scott-Tucker, A., Chaudhuri, R.R., Pallen, M.J., and Henderson, I.R. (2005b) Genomic analysis of the protein secretion systems in Clostridium acetobutylicum ATCC 824. Biochim Biophys Acta-Mol Cell Res 1745: 223-253.
16. Desvaux, M., Dumas, E., Chafsey, I., and Hébraud, M. (2006a) Protein cell surface display in Gram-positive bacteria: from single protein to macromolecular protein structure. FEMS Microbiol Lett 256: 1-15.
17. Desvaux, M., Hebraud, M., Henderson, I.R., and Pallen, M.J. (2006b) Type III secretion: what's in a name? Trends Microbiol 14: 157-160.
18. Desvaux, M., Cooper, L.M., Filenko, N.A., Scott-Tucker, A., Turner, S.M., Cole, J.A., and Henderson, I.R. (2006c) The unusual extended signal peptide region of the Type V secretion system is phylogenetically restricted. FEMS Microbiol Lett 264: 22-30.
19. Desvaux, M., Scott-Tucker, A., Turner, S.M., Cooper, L.M., Huber, D., Nataro, J.P., and Henderson, I.R. (2007) A conserved extended signal peptide region directs posttranslational protein translocation via a novel mechanism. Microbiology 153: 59-70.
20. Desvaux, M., Hébraud, M., Talon, R., and Henderson, I.R. (2009) Outer membrane translocation: numerical protein secretion nomenclature in question in mycobacteria. Trends Microbiol 17: 338-340.
21. Desvaux, M., Dumas, E., Chafsey, I., Chambon, C., and Hebraud, M. (2010) Comprehensive appraisal of the extracellular proteins from a monoderm bacterium: theoretical and empirical exoproteomes of Listeria monocytogenes EGD-e by secretomics. J Proteome Res 9: 5076-5092.
22. Djordjevic, D., Wiedmann, M., and McLandsborough, L.A. (2002) Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Appl Environ Microbiol 68: 2950-2958.
23. Du Plessis, D.J.F., Nouwen, N., and Driessen, A.J.M. (2011) The Sec translocase. Biochim et Biophys Acta-Biomembr 1808: 851-865.
24. Dumas, E., Desvaux, M., Chambon, C., and Hébraud, M. (2009) Insight into the core and variant exoproteomes of Listeria monocytogenes species by comparative subproteomic analysis. Proteomics 9: 3136-3155.
25. Dunne, W.M., Jr. (2002) Bacterial adhesion: seen any good biofilms lately? Clin Microbiol Rev 15: 155-166.
26. Farber, J.M., and Peterkin, P.I. (1991) Listeria monocytogenes, a food-borne pathogen. Microbiol Rev 55: 476-511.
27. Fortinea, N., Trieu-Cuot, P., Gaillot, O., Pellegrini, E., Berche, P., and Gaillard, J.L. (2000) Optimization of green fluorescent protein expression vectors for in vitro and in vivo detection of Listeria monocytogenes. Res Microbiol 151: 353-360.
28. Franciosa, G., Maugliani, A., Scalfaro, C., Floridi, F., and Aureli, P. (2009) Expression of internalin A and biofilm formation among Listeria monocytogenes clinical isolates. Int J Immunopathol Pharmacol 22: 183-193.
29. Franklin, M.J., Nivens, D.E., Weadge, J.T., and Howell, P.L. (2011) Biosynthesis of the Pseudomonas aeruginosa extracellular polysaccharides, alginate, Pel, and Psl. Front Microbiol 2: 167.
30. Gahan, C.G.M., and Collins, J.K. (1991) Listeriosis: biology and implications for the food industry. Trends Food Sci Technol 2: 89-93.
31. Geng, T., Kim, K.P., Gomez, R., Sherman, D.M., Bashir, R., Ladisch, M.R., and Bhunia, A.K. (2003) Expression of cellular antigens of Listeria monocytogenes that react with monoclonal antibodies C11E9 and EM-7G1 under acid-, salt- or temperature-induced stress environments. J Appl Microbiol 95: 762-772.
32. Giotis, E.S., Blair, I.S., and McDowell, D.A. (2007) Morphological changes in Listeria monocytogenes subjected to sublethal alkaline stress. Int J Food Microbiol 120: 250-258.
33. Giraud, C., and de Bentzmann, S. (2012) Inside the complex regulation of Pseudomonas aeruginosa chaperone usher systems. Environ Microbiol 14: 1805-1816.
34. Guedon, E., Desvaux, M., Payot, S., and Petitdemange, H. (1999) Growth inhibition of Clostridium cellulolyticum by an inefficiently regulated carbon flow. Microbiology 145: 1831-1838.
35. Guedon, E., Payot, S., Desvaux, M., and Petitdemange, H. (2000) Relationships between cellobiose catabolism, enzyme levels, and metabolic intermediates in Clostridium cellulolyticum grown in a synthetic medium. Biotechnol Bioeng 67: 327-335.
36. Halbedel, S., Hahn, B., Daniel, R.A., and Flieger, A. (2012) DivIVA affects secretion of virulence-related autolysins in Listeria monocytogenes. Mol Microbiol 83: 821-839.
37. Hall-Stoodley, L., and Stoodley, P. (2002) Developmental regulation of microbial biofilms. Curr Opin Biotechnol 13: 228-233.
38. Harmsen, M., Lappann, M., Knøchel, S., and Molin, S. (2010) Role of extracellular DNA during Biofilm formation by Listeria monocytogenes. Appl Environ Microbiol 76: 2271-2279.
39. Hazeleger, W.C., Dalvoorde, M., and Beumer, R.R. (2006) Fluorescence microscopy of NaCl-stressed, elongated Salmonella and Listeria cells reveals the presence of septa in filaments. Int J Food Microbiol 112: 288-290.
40. Heilmann, C. (2011) Adhesion mechanisms of staphylococci. Adv Exp Med Biol 715: 105-123.
41. Henderson, I.R., Owen, P., and Nataro, J.P. (1999) Molecular switches - the ON and OFF of bacterial phase variation. Mol Microbiol 33: 919-932.
42. de las Heras, A., Cain, R.J., Bieleckal, M.K., and Vazquez-Boland, J.A. (2011) Regulation of Listeria virulence: PrfA master and commander. Curr Opin Microbiol 14: 118-127.
43. Jørgensen, F., Stephens, P.J., and Knøchel, S. (1995) The effect of osmotic shock and subsequent adaptation on the thermotolerance and cell morphology of Listeria monocytogenes. J Appl Microbiol 79: 274-281.
44. 2 up- and downshift. Int J Food Microbiol 98: 145-155.
45. Kolter, R. (2005) Surfacing views of biofilm biology. Trends Microbiol 13: 1-2.
46. Korea, C.G., Badouraly, R., Prevost, M.C., Ghigo, J.M., and Beloin, C. (2010) Escherichia coli K-12 possesses multiple cryptic but functional chaperone-usher fimbriae with distinct surface specificities. Environ Microbiol 12: 1957-1977.
47. Lemon, K.P., Freitag, N.E., and Kolter, R. (2010) The virulence regulator PrfA promotes biofilm formation by Listeria monocytogenes. J Bacteriol 192: 3969-3976.
48. Lenz, L.L., and Portnoy, D.A. (2002) Identification of a second Listeria secA gene associated with protein secretion and the rough phenotype. Mol Microbiol 45: 1043-1056.
49. Lenz, L.L., Mohammadi, S., Geissler, A., and Portnoy, D.A. (2003) SecA2-dependent secretion of autolytic enzymes promotes Listeria monocytogenes pathogenesis. Proc Natl Acad Sci U S A 100: 12432-12437.
50. Longhi, C., Scoarughi, G.L., Poggiali, F., Cellini, A., Carpentieri, A., Seganti, L., etal. (2008) Protease treatment affects both invasion ability and biofilm formation in Listeria monocytogenes. Microb Pathog 45: 45-52.
51. de Luna, M.D., Scott-Tucker, A., Desvaux, M., Ferguson, P., Morin, N.P., Dudley, E.G., etal. (2008) The Escherichia coli biofilm-promoting protein Antigen 43 does not contribute to intestinal colonization. FEMS Microbiol Lett 284: 237-246.
52. Macé, C., Seyer, D., Chemani, C., Cosette, P., Di-Martino, P., Guery, B., etal. (2008) Identification of biofilm-associated cluster (bac) in Pseudomonas aeruginosa involved in biofilm formation and virulence. PLoS ONE 3: e3897.
53. Machata, S., Hain, T., Rohde, M., and Chakraborty, T. (2005) Simultaneous deficiency of both MurA and p60 proteins generates a rough phenotype in Listeria monocytogenes. J Bacteriol 187: 8385-8394.
54. Mackaness, G.B. (1964) The immunological basis of acquired cellular resistance. J Exp Med 120: 105-120.
55. Monk, I.R., Cook, G.M., Monk, B.C., and Bremer, P.J. (2004) Morphotypic conversion in Listeria monocytogenes biofilm formation: biological significance of rough colony isolates. Appl Environ Microbiol 70: 6686-6694.
56. Monk, I.R., Gahan, C.G., and Hill, C. (2008) Tools for functional postgenomic analysis of Listeria monocytogenes. Appl Environ Microbiol 74: 3921-3934.
57. Nilsson, R.E., Ross, T., and Bowman, J.P. (2011) Variability in biofilm production by Listeria monocytogenes correlated to strain origin and growth conditions. Int J Food Microbiol 150: 14-24.
58. Pilgrim, S., Kolb-Maurer, A., Gentschev, I., Goebel, W., and Kuhn, M. (2003) Deletion of the gene encoding p60 in Listeria monocytogenes leads to abnormal cell division and loss of actin-based motility. Infect Immun 71: 3473-3484.
59. Popowska, M. (2004) Analysis of the peptidoglycan hydrolases of Listeria monocytogenes: multiple enzymes with multiple functions. Pol J Microbiol 53 (Suppl.): 29-34.
60. Renier, S., Hébraud, M., and Desvaux, M. (2011) Molecular biology of surface colonization by Listeria monocytogenes: an additional facet of an opportunistic Gram-positive foodborne pathogen. Environ Microbiol 13: 835-850.
61. Renier, S., Micheau, P., Talon, R., Hébraud, M., and Desvaux, M. (2012) Subcellular localization of extracytoplasmic proteins in monoderm bacteria: rational secretomics-based strategy for genomic and proteomic analyses. PLoS ONE 7: e42982.
62. Renier, S., Chambon, C., Viala, D., Chagnot, C., Hebraud, M., and Desvaux, M. (2013) Exoproteomic analysis of the SecA2-dependent secretion in Listeria monocytogenes EGD-e. J Proteomics 80C: 183-195.
63. Rieu, A., Briandet, R., Habimana, O., Garmyn, D., Guzzo, J., and Piveteau, P. (2008) Listeria monocytogenes EGD-e biofilms: no mushrooms but a network of knitted chains. Appl Environ Microbiol 74: 4491-4497.
64. Rigel, N.W., and Braunstein, M. (2008) A new twist on an old pathway - accessory secretion systems. Mol Microbiol 69: 291-302.
65. Rossiter, A.E., Browning, D.F., Leyton, D.L., Johnson, M.D., Godfrey, R.E., Wardius, C.A., etal. (2011) Transcription of the plasmid-encoded toxin gene from enteroaggregative Escherichia coli is regulated by a novel co-activation mechanism involving CRP and Fis. Mol Microbiol 81: 179-191.
66. Rowan, N.J., Candlish, A.A., Bubert, A., Anderson, J.G., Kramer, K., and McLauchlin, J. (2000) Virulent rough filaments of Listeria monocytogenes from clinical and food samples secreting wild-type levels of cell-free p60 protein. J Clin Microbiol 38: 2643-2648.
67. Sambrook, J., and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual. New York, NY, USA: Cold Spring Harbor.
68. Sasahara, K.C., and Zottola, E.A. (1993) Biofilm formation by Listeria monocytogenes utilizes a primary colonizing microorganism in flowing system. J Food Prot 56: 1022-1028.
69. Smoot, L.M., and Pierson, M.D. (1998) Influence of environmental stress on the kinetics and strength of attachment of Listeria monocytogenes Scott A to Buna-N rubber and stainless steel. J Food Prot 61: 1286-1292.
70. Szlavik, J., Paiva, D.S., Mork, N., van den Berg, F., Verran, J., Whitehead, K., etal. (2012) Initial adhesion of Listeria monocytogenes to solid surfaces under liquid flow. Int J Food Microbiol 152: 181-188.
71. Toledo-Arana, A., Dussurget, O., Nikitas, G., Sesto, N., Guet-Revillet, H., Balestrino, D., etal. (2009) The Listeria transcriptional landscape from saprophytism to virulence. Nature 459: 950-956.
72. Travier, L., Guadagnini, S., Gouin, E., Dufour, A., Chenal-Francisque, V., Cossart, P., etal. (2013) ActA promotes Listeria monocytogenes aggregation, intestinal colonization and carriage. PLoS Pathog 9: e1003131.
73. van der Veen, S., van Schalkwijk, S., Molenaar, D., de Vos, W.M., Abee, T., and Wells-Bennik, M.H.J. (2010) The SOS response of Listeria monocytogenes is involved in stress resistance and mutagenesis. Microbiology-Sgm 156: 374-384.
74. Young, J.M., Leschine, S.B., and Reguera, G. (2012) Reversible control of biofilm formation by Cellulomonas spp. in response to nitrogen availability. Environ Microbiol 14: 594-604.