Vibrio splendidus persister cells induced by host coelomic fluids show a similar phenotype to antibiotic-induced counterparts.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
09 2021
09 2021
Historique:
revised:
28
07
2021
received:
15
06
2021
accepted:
10
08
2021
pubmed:
15
8
2021
medline:
15
12
2021
entrez:
14
8
2021
Statut:
ppublish
Résumé
Persister cells are dormant variants of regular cells that are multidrug tolerant and have heterogeneous phenotypes; these cells are a potential threat to hosts because they can escape the immune system or antibiotic treatments and reconstitute infectious. Skin ulcer syndrome (SUS) frequently occurs in the sea cucumber (Apostichopus japonicus), and Vibrio splendidus is one of the main bacterial pathogens of SUS. This study found that the active cells of V. splendidus became persister cells more readily in the presence of A. japonicus coelomic fluids. We showed that the A. japonicus coelomic fluids plus antibiotics induce 100-fold more persister cells in V. splendidus compared with antibiotics alone via nine sets of experiments including assays for antibiotic resistance, metabolic activity, and single-cell phenotypes. Furthermore, the coelomic fluids-induced persister cells showed similar phenotypes as the antibiotic-induced persister cells. Further investigation showed that guanosine pentaphosphate/tetraphosphate (henceforth ppGpp) and SOS response pathway involved in the formation of persister cells as determined using real-time RT-PCR. In addition, single-cell observations showed that, similar to the antibiotic-induced V. splendidus persister cells, the coelomic fluids-induced persister cells have five resuscitation phenotypes: no growth, expansion, elongation, elongation and then division, and elongation followed by death/disappearance. In addition, dark foci formed in the majority of persister cells for both the antibiotic-induced and coelomic fluids-induced persister cells. Our results highlight that the pathogen V. splendidus might escape from the host immune system by entering the persister state during the process of infection due to exposure to coelomic fluids.
Identifiants
pubmed: 34390618
doi: 10.1111/1462-2920.15717
doi:
Substances chimiques
Anti-Bacterial Agents
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
5605-5620Informations de copyright
© 2021 Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Ayrapetyan, M., Williams, T.C., and Oliver, J.D. (2015a) Bridging the gap between viable but non-culturable and antibiotic persistent bacteria. Trends Microbiol 23: 7-13.
Ayrapetyan, M., Williams, T.C., Baxter, R., and Oliver, J.D. (2015b) Viable but nonculturable and persister cells coexist stochastically and are induced by human serum. Infect Immun 83: 4194-4203.
Bakkeren, E., Huisman, J.S., Fattinger, S.A., Hausmann, A., Furter, M., Egli, A., et al. (2019) Salmonella persisters promote the spread of antibiotic resistance plasmids in the gut. Nature 573: 276-280.
Balaban, N.Q. (2011) Persistence: mechanisms for triggering and enhancing phenotypic variability. Curr Opin Genet Dev 21: 768-775.
Binesse, J., Delsert, C., Saulnier, D., Champomier-Verges, M.C., Zagorec, M., Munier-Lehmann, H., et al. (2008) MetalloproteaseVsm is the major determinant of toxicity for extracellular products of Vibrio splendidus. Appl Environ Microbiol 74: 7108-7117.
Bui, L.M., Conlon, B.P., and Kidd, S.P. (2017) Antibiotic tolerance and the alternative lifestyles of Staphylococcus aureus. Essays Biochem 61: 71-79.
Cao, R., Wang, Q., Yang, D., Liu, Y., Ran, W., Qu, Y., et al. (2018) CO2-induced ocean acidification impairs the immune function of the Pacific oyster against Vibrio splendidus challenge: an integrated study from a cellular and proteomic perspective. Sci Total Environ 625: 1574-1583.
Cho, J., Carr, A.N., Whitworth, L., Johnson, B., and Wilson, K.S. (2017) MazEF toxin-antitoxin proteins alter Escherichia coli cell morphology and infrastructure during persister formation and regrowth. Microbiology (Reading) 163: 308-321.
Chung, H.S., Yao, Z., Goehring, N.W., Kishony, R., Beckwith, J., and Kahne, D. (2009) Rapid beta-lactam-induced lysis requires successful assembly of the cell division machinery. Proc Natl Acad Sci U S A 106: 21872-21877.
Cui, P., Niu, H., Shi, W., Zhang, S., Zhang, W., and Ying, Z. (2018) Identification of genes involved in bacteriostatic antibiotic-induced persister formation. Front Microbiol 9: 413.
Dhillon, J., Fourie, P.B., and Mitchison, D.A. (2014) Persister populations of mycobacterium tuberculosis in sputum that grow in liquid but not on solid culture media. J Antimicrob Chemother 69: 437-440.
Dong, K., Pan, H., Yang, D., Rao, L., Zhao, L., Wang, Y., et al. (2020) Induction, detection, formation, and resuscitation of viable but non-culturable state microorganisms. Compr Rev Food Sci Food Saf, 19: 149-183.
Fauvart, M., de Groote, V.N., and Michiels, J. (2011) Role of persister cells in chronic infections: clinical relevance and perspectives on anti-persister therapies. J Med Microbiol 60: 699-709.
Fisher, R.A., Gollan, B., and Helaine, S. (2017) Persistent bacterial infections and persister cells. Nat Rev Microbiol 15: 453-464.
Goormaghtigh, F., Fraikin, N., Putrinš, M., Hallaert, T., Hauryliuk, V., Garcia-Pino, A., et al. (2018) Reassessing the role of type ii toxin-antitoxin systems in formation of Escherichia coli type ii persister cells. mBio 9: e00640-e00618.
González, R., Brokordt, K., Cárcamo, C.B., Coba, T., Oyanedel, D., Mercado, L., et al. (2017) Molecular characterization and protein localization of the antimicrobial peptide big defensin from the scallop Argopecten purpuratus after Vibrio splendidus challenge. Fish Shellfish Immunol 68: 173-179.
Grassi, L., Di Luca, M., Maisetta, G., Rinaldi, A.C., Esin, S., Trampuz, A., and Batoni, G. (2017) Generation of persister cells of Pseudomonas aeruginosa and Staphylococcus aureus by chemical treatment and evaluation of their susceptibility to membrane-targeting agents. Front Microbiol 8: 1917.
Helaine, S., Cheverton, A.M., Watson, K.G., Faure, L.M., Matthews, S.A., and Holden, D.W. (2014) Internalization of salmonella by macrophages induces formation of nonreplicating persisters. Science 343: 204-208.
Huq, A., Whitehouse, C.A., Grim, C.J., Alam, M., and Colwell, R.R. (2008) Biofilms in water, its role and impact in human disease transmission. Curr Opin Biotechnol 19: 244-247.
Jiang, J., Zhao, Z., Pan, Y., Dong, Y., Gao, S., Jiang, B., et al. (2020) Proteomics reveals the gender differences in humoral immunity and physiological characteristics associated with reproduction in the sea cucumber Apostichopus japonicus. J Proteomics 217: 103687.
Jiang, J., Zhou, Z., Dong, Y., Zhao, Z., Sun, H., Wang, B., et al. (2017) Comparative expression analysis of immune-related factors in the sea cucumber Apostichopus japonicus. Fish Shellfish Immunol 72: 342-347.
Jin, X., Kightlinger, W., Kwon, Y.-C., and Hong, S.H. (2018) Rapid production and characterization of antimicrobial colicins using Escherichia coli-based cell-free protein synthesis. Synthetic Biology 3: ysy004.
Johnson, P.J.T., and Levin, B.R. (2013) Pharmacodynamics, population dynamics, and the evolution of persistence in Staphylococcus aureus. PLoS Genet 9: e1003123.
Kim, J.S., Yamasaki, R., Song, S., Zhang, W., and Wood, T.K. (2018) Single cell observations show persister cells wake based on ribosome content. Environ Microbiol 20: 2085-2098.
Kwan, B.W., Valenta, J.A., Benedik, M.J., and Wood, T.K. (2013) Arrested protein synthesis increases persister-like cell formation. Antimicrob Agents Chemother 57: 1468-1473.
Le, R.F., Binesse, J., Saulnier, D., and Mazel, D. (2007) Constructionof a Vibrio splendidus mutant lacking the metalloprotease gene vsm by use of a novel counterselectable suicide vector. Appl Environ Microbiol 73: 777-784.
Lewis, K. (2005) Persister cells and the riddle of biofilm survival. Biochemistry (Mosc) 70: 267-274.
Li, Y., and Zhang, Y. (2007) PhoU is a persistence switch involved in persister formation and tolerance to multiple antibiotics and stresses in Escherichia coli. Antimicrob Agents Chemother 51: 2092-2099.
Liu, H., Zheng, F., Sun, X., Hong, X., Dong, S., Wang, B., et al. (2010) Identification of the pathogens associated with skin ulceration and peristome tumescence in cultured sea cucumbers Apostichopus japonicus (Selenka). J Invertebr Pathol 105: 236-242.
Liu, R., Chen, H., Zhang, R., Zhou, Z., Hou, Z.H., Gao, D.H., et al. (2016) The comparative transcriptome analysis of Vibrio splendidus Z6 revealed the mechanism of its pathogenicity at low temperature. Appl Environ Microbiol 82: 2050-2061.
Long, Y., Fu, W., Li, S., Ren, H., Li, M., Liu, C., et al. (2019) Identification of novel genes that promote persister formation by repressing transcription and cell division in Pseudomonas aeruginosa. J Antimicrob Chemother 74: 2575-2587.
Maisonneuve, E., and Gerdes, K. (2014) Molecular mechanisms underlying bacterial persisters. Cell 157: 539-548.
Maisonneuve, E., Castro-Camargo, M., and Gerdes, K. (2018) (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 172: 1135.
Martins, D., McKay, G.A., English, A.M., and Nguyen, D. (2020) Sublethal paraquat confers multidrug tolerance in Pseudomonas aeruginosa by inducing superoxide dismutase activity and lowering envelope permeability. Front Microbiol 11: 576708.
Michiels, J.E., van den Bergh, B., Verstraeten, N., and Michiels, J. (2016) Molecular mechanisms and clinical implications of bacterial persistence. Drug Resist Updat 29: 76-89.
Möker, N., Dean, C.R., and Tao, J. (2010) Pseudomonas aeruginosa increases formation of multidrug-tolerant persister cells in response to quorum-sensing signaling molecules. J Bacteriol 192: 1946-1955.
Narayanaswamy, V.P., Keagy, L.L., Duris, K., Wiesmann, W., Loughran, A.J., Townsend, S.M., et al. (2018) Novel glycopolymer eradicates antibiotic- and CCCP-induced persistercells in Pseudomonas aeruginosa. Front Microbiol 9: 1724.
Pont, S., Fraikin, N., Caspar, Y., Van, M.L., Attrée, I., and Cretin, F. (2020) Bacterial behavior in human blood reveals complement evaders with some persister-like features. PLoS Pathog 16: e1008893.
Pu, Y., Li, Y., Jin, X., Tian, T., Ma, Q., Zhao, Z.Y., et al. (2019) ATP-dependent dynamic protein aggregation regulates bacterial dormancy depth critical for antibiotic tolerance. Mol Cell 73: 143, e4-156.
Putrinš, M., Kogermann, K., Lukk, E., Lippus, M., Varik, V., Tenson, T., et al. (2015) Phenotypic heterogeneity enables uropathogenic Escherichia coli to evade killing by antibiotics and serum complement. Infect Immun 83: 1056-1067.
Yee, R., Yuting, Y., Shi, W., Brayton, C., Tarff, A., Fen, J., et al. (2019) Infection with persister forms of Staphylococcus aureus causes a persistent skin infection with more severe lesions in mice: failure to clear the infection by the current standard of care treatment. Discov Med 28: 7-16.
Rowe, S.E., Wagner, N.J., Li, L., Beam, J.E., Wilkinson, A.D., Radlinski, L.C., et al. (2020) Reactive oxygen species induce antibiotic tolerance during systemic Staphylococcus aureus infection. Nat Microbiol 5: 282-290.
Sanders, C.C. (1988) Ciprofloxacin: in vitro activity, mechanism of action, and resistance. Rev Infect Dis 10: 516-527.
Siibak, T., Peil, L., Xiong, L., Mankin, A., and Tenson, T. (2009) Erythromycin-and chloramphenicol-induced ribosomal assembly defects are secondary effects of protein synthesis inhibition. Antimicrob Agents Chemother 53: 563-571.
Silva-Valenzuela, C.A., Lazinski, D.W., Kahne, S.C., Nguyen, Y., Molina-Quiroz, R.C., and Camilli, A. (2017) Growth arrest and a persister state enable resistance to osmotic shock and facilitate dissemination of Vibrio cholerae. ISME J 11: 2718-2728.
Skurnik, D., Roux, D., Cattoir, V., Da Nilchanka, O., Lu, X., Yoder-Himes, D.R., et al. (2013) Enhanced in vivo fitness of carbapenem-resistant oprD mutants of Pseudomonas aeruginosa revealed through high-throughput sequencing. Proc Natl Acad Sci U S A 110: 20747-20752.
Song, S., and Wood, T.K. (2021) 'Viable but non-culturable cells' are dead. Environ Microbiol 23: 2335-2338.
Song, S., and Wood, T.K. (2020) ppGpp ribosome dimerization model for bacterial persister formation and resuscitation. Biochem Biophys Res Commun 523: 281-286.
Stapels, D.,.A.C., Hill, P.,.W.S., Westermann, A.J., Fisher, R.,.A., Thurston, T.,.L., Saliba, A.-E., et al. (2018) Salmonella persisters undermine host immune defenses during antibiotic treatment. Science 362: 1156-1160.
Sulaiman, J.E., Hao, C., and Lam, H. (2018) Specific enrichment and proteomics analysis of Escherichia coli persisters from rifampin pretreatment. J Proteome Res 17: 3984-3996.
Sun, F., Bian, M., Li, Z., Lv, B., Gao, Y., Wang, Y., and Fu, X. (2020) 5-methylindole potentiates aminoglycoside against gram-positive bacteria including Staphylococcus aureus persisters under hypoionic conditions. Front Cell Infect Microbiol 10: 84.
Thomson, R., Macpherson, H.L., Riaza, A., and Birkbeck, T.H. (2005) Vibrio splendidus biotype 1 as a cause of mortalities in hatchery-reared larval turbot, Scophthalmus maximus (L.). J Appl Microbiol 99: 243-250.
Tkhilaishvili, T., Lombardi, L., Klatt, A.-B., Trampuz, A., and Di, L.M. (2018) Bacteriophage Sb-1 enhances antibiotic activity against biofilm, degrades exopolysaccharide matrix and targets persisters of Staphylococcus aureus. Int J Antimicrob Agents 52: 842-853.
Toprak, E., Veres, A., Michel, J.-B., Chait, R., Hartl, D.L., and Roy, K. (2011) Evolutionary paths to antibiotic resistance under dynamically sustained drug selection. Nat Genet 44: 101-105.
Torresi, M., Acciari, V.A., Piano, A., Serratore, P., Prencipe, V., and Migliorati, G. (2011) Detection of Vibrio splendidus and related species in Chamelea gallina sampled in the adriatic along the abruzzi coastline. Vet Ital 47: 363-370.
The VibrioSea Consortium, Vezzulli, L., Pezzati, E., Moreno, M., Fabiano, M., Pane, L., and Pruzzo, C. (2009) Benthic ecology of vibrio spp. and pathogenic vibrio species in a coastal mediterranean environment (La Spezia gulf, Italy). Microb Ecol 58: 808-818.
Wilmaerts, D., Windels, E.M., Verstraeten, N., and Michiels, J. (2019) General mechanisms leading to persister formation and awakening. Trends Genet 35: 401-411.
Wood, T.K., Song, S., and Yamasaki, R. (2019) Ribosome dependence of persister cell formation and resuscitation. J Microbiol 57: 213-219.
Yao, Z., Kahne, D., and Kishony, R. (2012) Distinct single-cell morphological dynamics under beta-lactam antibiotics. Mol Cell 48: 705-712.
Yu, J., Yang, L., Yin, H., and Chang, Z. (2019) Regrowth-delay body as a bacterial subcellular structure marking multidrug-tolerant persisters. Cell Discov 5: 8.
Yu, W., Li, D., Li, H., Tang, Y., Tang, H., Ma, X., et al. (2020) Absence of tmRNA increases the persistence to cefotaxime and the intercellular accumulation of metabolite glcNAc in Aeromonas veronii. Front Cell Infect Microbiol 10: 44.
Zeng, B., Zhao, G., Cao, X., Yang, Z., Wang, C., and Hou, L. (2013) Formation and resuscitation of viable but nonculturable Salmonella typhi. Biomed Res Int 2013: 907170.
Zhang, C., Liang, W., Zhang, W., and Li, C. (2016a) Characterization of a metalloprotease involved in Vibrio splendidus infection in the sea cucumber, Apostichopus japonicus. Microb Pathog 101: 96-103.
Zhang, W., Li, C. (2021). Virulence mechanisms of vibrios belonging to the Splendidus clade as aquaculture pathogens, from case studies and genome data. Reviews in Aquaculture. http://dx.doi.org/10.1111/raq.12555
Zhang, W., Liang, W., and Li, C. (2016b) Inhibition of marine Vibrio spp. by pyoverdine from Pseudomonas aeruginosa PA1. J Hazard Mater 302: 217-224.
Zhang, W., Yamasaki, R., Song, S., and Wood, T.K. (2019) Interkingdom signal indole inhibits Pseudomonas aeruginosa persister cell waking. J Appl Microbiol 127: 1768-1775.
Zhang, Y. (2014) Persisters, persistent infections and the Yin-Yang model. Emerg Microbes Infect 3: e3.
Zhao, Y., Lv, B., Sun, F., Liu, J., Wang, Y., Gao, Y., et al. (2020) Rapid freezing enables aminoglycosides to eradicate bacterial persisters via enhancing mechanosensitive channel mscL-mediated antibiotic uptake. mBio 11: e03239-03219.
Zheng, E.J., Stokes, J.M., and Collins, J.J. (2020) Eradicating bacterial persisters with combinations of strongly and weakly metabolism-dependent antibiotics. Cell Chem Biol 27: 1544-1552.