Abstract—
Lactic acid bacteria (LAB) are important components of the human microbiome. While they are capable both of synthesis and response to the signals of the human humoral regulatory system (hormones and neuromediators), the phenomenology and mechanisms of the LAB response to these mediators are insufficiently studied. This work showed estrogen to hinder the growth and development of E. durans, while norepinephrine, estrogen, and the brain natriuretic peptide caused dose-dependent extension of the stationary growth phase. This is the first report on stimulation of E. durans biofilm formation by the atrial natriuretic peptide and estrogen. The frequency of persister formation depended on the type of bacterial growth (planktonic or biofilm one) and was higher in the case of biofilm growth. Epinephrine and norepinephrine exhibited dose-dependent stimulation of persister formation in planktonic LAB cultures, while other tested hormones inhibited it. The effect on persister formation in biofilms was different: natriuretic peptides exhibited dose-dependent stimulation of persister formation, and none of the hormones inhibited it significantly. After several months of incubation, E. durans persister cells matured to anabiotic dormant forms with the typical ultrastructural features. The population of E. durans dormant forms was first shown to contain the form with different dormancy depth, including the viable uncultured ones.
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REFERENCES
Ayrapetyan, M., Williams, T., and Oliver, J.D., Bridging the gap between viable but non-culturable and antibiotic persistent bacteria, Trends Microbiol., 2015, vol. 23, pp. 7–13. https://doi.org/10.1016/j.tim.2014.09.004
Ayrapetyan, M., Williams, T., and Oliver, J.D., Relationship between the viable but nonculturable state and antibiotic persister cells, J. Bacteriol., 2018, vol. 200, art. e00249-18. https://doi.org/10.1128/JB.00249-18
Bacteria as Multicellular Organisms, Shapiro, J.A. and Dworkin, M., Eds., Oxford Univ. Press, 1997.
Balaban, N., Merrin, I., Chait, R., Kowalik, L., and Leibler, S., Bacterial persistence as a phenotypic switch, Science, 2004, vol. 305, pp. 1622‒1625.
Balaban, N.Q., Helaine, S., Lewis, K., Ackermann, M., Aldridge, B., Andersson, D.I., Brynildsen, M.P., Bumann, D., Camilli, A., Collins, J.J., Dehio, C., Fortune, S., Ghigo, J.-M., Hardt, W.-D., Harms, A., et al., Definitions and guidelines for research on antibiotic persistence, Nat. Rev. Microbiol., 2019, vol. 17, pp. 441–448. https://doi.org/10.1038/s41579-019-0196-3
Baquero, F. and Levin, B.R., Proximate and ultimate causes of the bactericidal action of antibiotics, Nat. Rev. Microbiol., 2021, vol. 19, pp. 123–132. https://doi.org/10.1038/s41579-020-00443-1
Bigger, J.W., Treatment of staphylococcal infections with penicillin by intermittent sterilisation, Lancet, 1944, vol. 244, pp. 497–500. https://doi.org/10.1016/S0140-6736(00)74210-3
Bukharin, O.V., Gintsburg, A.L., Romanova, Yu.M., and El’-Registan, G.I., Mekhanizmy vyzhivaniya bakterii (Mechanisms of Bacterial Survival), Moscow: Meditsina, 2005.
Canas-Duarte, S.J., Restrepo, S., and Pedraza, J.M., Novel protocol for persister cells isolation, PLoS One, 2014, vol. 9, art. e88660. https://doi.org/10.1371/journal.pone.0088660
Chebotar, I.V., Emelyanova, M.A., Bocharova, J.A., Mayansky, N.A., Kopantseva, E.E., and Mikhailovich, V.M., The classification of bacterial survival strategies in the presence of antimicrobials, Microb. Pathog., 2021, vol. 155, art. 104901. https://doi.org/10.1016/j.micpath.2021.104901
Colwell, R.R., Brayton, P.R., Grimes, D.J., Roszak, D.B., Huq, S.A., and Palmer, L.M., Viable but non-culturable Vibrio cholerae and related pathogens in the environment: implications for release of genetically engineered microorganisms, Nat. Biotechnol., 1985, vol. 3, pp. 817–820. https://doi.org/10.1038/nbt0985-817
Dadinova, L.A., Chesnokov, Y.M., Kamyshinsky, R.A., Orlov, I.A., Petoukhov, M.V., Mozhaev, A.A., Soshins-kaya, E.Yu., Lazarev, V.N., Manuvera, V.A., Orekhov, A.S., Vasiliev, A.L., and Shtykova, E.V., Protective Dps-DNA co-crystallization in stressed cells: an in vitro structural study by small-angle X-ray scattering and cryo-electron tomography, FEBS Lett., 2019, vol. 593, pp. 1360‒1371. https://doi.org/10.1002/1873-3468.13439
El-Registan, G.I., Mulyukin, A.L., Nikolaev, Yu.A., Gal’chenko, V.F., Suzina, N.E., and Duda, V.I., Adaptogenic functions of extracellular autoregulators of microorganisms, Microbiology (Moscow), 2006, vol. 75, pp. 380‒389.
Fuqua, W.C., Winans, S.C., and Greenberg, E.P., Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators, J. Bacteriol., 1994, vol. 176, pp. 269–275.
Golod, N.A., Loiko, N.G., Mulyukin, A.L., Neiymatov, A.L., Vorobjeva, L.I., Suzina, N.E., Shanenko, E.F., Gal’chenko, V.F., and El-Registan, G.I., Adaptation of lactic acid bacteria to unfavorable growth conditions, Microbiology (Moscow), 2009, vol. 78, pp. 280‒289.
Kaldalu, N., Hauryliuk, V., Turnbull, K.J., La Mensa, A., Putrinš, M., and Tenson, T., In vitro studies of persister cells, Microbiol. Mol. Biol. Rev., 2020, vol. 84, art. e00070-20. https://doi.org/10.1128/MMBR.00070-20
Kaldalu, N., Joers, A., Ingelman, H., and Tenson, T., A general method for measuring persister levels in Escherichia coli cultures, Methods Mol. Biol., 2016, vol. 1333, pp. 29–42. https://doi.org/10.1007/978-1-4939-2854-5_3
Kaprelyants, A.S., Mukamolova, G.V., and Kell, D.B., Estimation of dormant Micrococcus luteus cells by penicillin lysis and by resuscitation in cellfree spent medium at high dilution, FEMS Microbiol. Lett., 1994, vol. 115, pp. 347–352.
Kaushik, V., Sharma, S., Tiwari, M., and Tiwari, V., Antipersister strategies against stress induced bacterial persistence, Microb. Pathog., 2022, vol. 164, art. 105423. https://doi.org/10.1016/j.micpath.2022.105423
Kell, D.B., Kaprelyants, A.S., Weichart, D.H., Harwood, C.R., and Barer, M.R., Viability and activity in readily culturable bacteria: a review and discussion of the practical issues, Antonie van Leeuwenhoek, 1998, vol. 73, pp. 169–187. https://doi.org/10.1023/A:1000664013047
Kim, J.S., Chowdhury, N., Yamasaki, R., and Wood, T.K., Viable but non-culturable and persistence describe the same bacterial stress state, Environ. Microbiol., 2018, vol. 20, pp. 2038–2048. https://doi.org/10.1111/1462-2920.14075
Krawczyk, A.O., de Jong, A., Omony, J., Holsappel, S., Wells-Bennik, M.H.J., Kuipers, O.P., and Eijlander, R.T., Spore heat activation requirements and germination responses correlate with sequences of germinant receptors and with the presence of a specific spoVA2mob operon in foodborne strains of Bacillus subtilis, Appl. Environ. Microbiol., 2017, vol. 83. https://doi.org/10.1128/AEM.03122-16
Lewis, K., Persister cells, Annu. Rev. Microbiol., 2010, vol. 64, pp. 357‒372.
Loiko, N.G., Kozlova, A.N., Nikolaev, Y.A., Gaponov, A.M., Tutel’yan, A.V., and El’-Registan, G.I., Effect of stress on emergence of antibiotic-tolerant Escherichia coli cells, Microbiology (Moscow), 2015, vol. 84, pp. 595‒609.
Loiko, N.G., Krasnova, M.A., Pichugina, T.V., Gr-inevich, A.I., Ganina, V.I., Kozlova, A.N., Niko-laev, Yu.A., Gal’chenko, V.F., and El’-Registan, G.I., Changes in the phase variant spectra in the populations of lactic acid bacteria under antibiotic treatment, Microbiology (Moscow), 2014, vol. 83, pp. 195‒204.
Lyte, M., Microbial endocrinology and nutrition: a perspective on new mechanisms by which diet can influence gut-to brain-communication, PharmaNutrition, 2013, vol. 1, pp. 35‒39.
Lyte, M., The effect of stress on microbial growth, Anim. Health Res. Rev., 2014, vol. 15, pp. 172‒174. https://doi.org/10.1017/S146625231400019X
Lyte, M., The microbial organ in the gut as a driver of homeostasis and disease, Med. Hypotheses, 2010, vol. 74, pp. 634–638.
Maisonneuve, E. and Gerdes, K., Molecular mechanisms underlying bacterial persisters, Cell, 2014, vol. 157, pp. 539–548. https://doi.org/10.1016/j.cell.2014.02.050
Markova, N., Slavchev, G., Michailova, L., and Jourdanova, M., Survival of Escherichia coli under lethal heat stress by L-form conversion, Int. J. Biol. Sci., 2010, vol. 6, pp. 303‒315. https://doi.org/10.7150/ijbs.6.303
Mukamolova, G.V., Kaprelyants, A.S., and Kell, D.B., Secretion of an antibacterial factor during resuscitation of dormant cells in Micrococcus luteus cultures held in an extended stationary phase, Antonie Van Leeuwenhoek, 1995, vol. 67, pp. 289–295.
Mulyukin, A.L., Pogorelova, A.Yu., El-Registan, G.I., Suzina, N.E., Duda, V.I., and Antonyuk, L.P., Diverse morphological types of dormant cells and conditions for their formation in Azospirillum brasilense, Microbiology (Moscow), 2009, vol. 78, pp. 33‒41.
Mulyukin, A.L., Suzina, N.E., Mel’nikov, V.G., Gal’chenko, V.F., and El’-Registan, G.I., Dormant state and phenotypic variability of Staphylococcus aureus and Corynebacterium pseudodiphtheriticum, Microbiology (Moscow), 2014, vol. 83, pp. 149‒159.
Oleskin, A.V., El’-Registan, G.I., and Shenderov, B.A., Role of neuromediators in the functioning of the human microbiota: “business talks” among microorganisms and the microbiota-host dialogue, Microbiology (Moscow), 2016, vol. 85, pp. 1‒22.
Oleskin, A.V., Kirovskaya, T.A., Botvinko, I.V., and Lysak, L.V., Effects of serotonin (5-hydroxytryptamine) on the growth and differentiation of microorganisms, Microbiology (Moscow), 1998, vol. 67, pp. 251‒257.
Oleskin, A.V., Shenderov, B.A., and Rogovskii, V.S., Sotsial’nost’ mikroorganizmov i vzaimootnosheniya v sisteme mikrobiota−khozyain: rol’ neiromediatorov (Sociality of Microorganisms and Relations in the Microbiota-Host System: Role of Neuromediators), Moscow: Mos. Gos. Univ., 2020.
O’Toole, G.A., Microtiter dish biofilm formation assay, J. Visual. Exper., 2011, vol. 47, p. 2437.
Pogorelova, A.Y., Mulyukin, A.L., Galchenko, V.F., El’-Registan, G.I., and Antonyuk, L.P., Phenotypic variability in Azospirillum brasilense strains Sp7 and Sp245: association with dormancy and characteristics of the variants, Microbiology (Moscow), 2009, vol. 78, pp. 559‒568.
Salina, E.G., Grigorov, A.S., Bychenko, O.S., Skvortsova, Y.V., Mamedov, I.Z., Azhikina, T.L., and Kaprelyants, A.S., Resuscitation of dormant “non-culturable” Mycobacterium tuberculosis is characterized by immediate transcriptional burst, Front. Cell Infect. Microbiol., 2019, vol. 9, p. 272. https://doi.org/10.3389/fcimb.2019.00272
Shleeva, M.O., Salina, E.G., and Kaprelyants, A.S., Dormant forms of mycobacteria, Microbiology (Moscow), 2010, vol. 79, pp. 1‒12.
Song, S. and Wood, T.K., “Viable but non-culturable cells” are dead, Environ. Microbiol., 2021, vol. 23, pp. 2335–2338. https://doi.org/10.1111/1462-2920.15463
Strahl, H. and Errington, J., Bacterial membranes: structure, domains, and function, Annu. Rev. Microbiol., 2017, vol. 71, pp. 519–538.
Svenningsen, M.S., Veress, A., Harms, A., Mitarai, N., and Semsey, S., Birth and resuscitation of (p)ppGpp induced antibiotic tolerant persister cells, Sci. Rep., 2019, vol. 9, art. 6056. https://doi.org/10.1038/s41598-019-42403-7
Van den Bergh, B., Fauvart, M., and Michiels, J., Formation, physiology, ecology, evolution and clinical importance of bacterial persisters, FEMS Microbiol. Rev., 2017, vol. 41, pp. 219‒251. https://doi.org/10.1093/femsre/fux001
Wainwright, J., Hobbs, G., and Nakouti, I., Persister cells: formation, resuscitation and combative therapies, Arch. Microbiol., 2021, vol. 203, pp. 5899–5906. https://doi.org/10.1007/s00203-021-02585-z
Wiradiputra, M.R.D., Khuntayaporn, P., Thirapanmethee, K., and Chomnawang, M.T., Toxin-antitoxin systems: a key role on persister formation in Salmonella enterica serovar typhimurium, Infect. Drug Resist., 2022, vol. 15, pp. 5813–5829. https://doi.org/10.2147/IDR.S378157
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Electron microscopy was carried out using the equipment of the UNIQEM Microbial Collection Joint Use Center, Research Center of Biotechnology, Russian Academy of Sciences.
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The work was supported by the Ministry of Science and Higher Education of the Russian Federation.
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El’-Registan, G.I., Zemskova, O.V., Galuza, O.A. et al. Effect of Hormones and Biogenic Amines on Growth and Survival of Enterococcus durans. Microbiology 92, 517–533 (2023). https://doi.org/10.1134/S0026261723600866
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DOI: https://doi.org/10.1134/S0026261723600866