Evaluation of Proteins Released to Medium in Yeast-Bacteria Co-culture System

Yıl 2023, , 488 - 498, 30.06.2023

Ayşegül Yanık , Çağatay Tarhan

https://doi.org/10.28979/jarnas.1196962

Öz

Cultivation of microorganisms in ideal laboratory conditions seperates them from their natural conditions and isolates them from their microbial world, especially from their competitors. With traditional pure culture-oriented cultuvation techniques, interactions mediated by small molecules are not taken into account, resulting in the precise nature of the interactions being largely unknown. Co-culture systems are systems in which two or more different cell populations are grown together. In this way, studies on natural interactions between populations can be made and synthetic interactions that are not observed in nature can be provided. With these systems, natural product discovery, microbial ecology, evolution and pathogenesis studies are carried out. In addition, co-culture systems are also used in industrial, environmental and medical studies. In this study, the wild strain of Schizosaccharomyces pombe and the DH5α strain of Escherichia coli were grown in their own specific media, then cultured for 48 hours and 72 hours by cultivating in media containing 0,1% glucose with different cell number, and finally the differentiation in the proteins released by the cells into the medium was observed in SDS polyacrylamide gels. Different from the control conditions, new protein bands that emerged under the co-culture conditions were detected and two of these bands were analyzed by mass spectrometry (MS). While 6 of differentaited proteins were released by S.pombe, 257 proteins matched with E.coli proteom. These proteins are; Various carbohydrate-binding proteins, membrane proteins involved in the identification of various signaling molecules and antibiotics, and other proteins involved in various cellular processes.

Anahtar Kelimeler

Co-culture, Escherichia coli., proteomics, Shizosaccharomyces pombe

Destekleyen Kurum

İstanbul Üniversitesi Bilimsel Araştırma Projeleri Birimi

Proje Numarası

33600

Teşekkür

This study was supported by Istanbul University Scientific Research Projects Unit (BAP) with project number 33600. We thank BAP for their support.

Kaynakça

• Ackerley, D. F., Gonzalez, C. F., Park, C. H., Blake, R., 2nd, Keyhan, M., & Matin, A. (2004). Chromate-reducing properties of soluble flavoproteins from Pseudomonas putida and Escherichia coli. Applied and environmental microbiology, 70(2), 873–882. https://doi.org/10.1128/AEM.70.2.873-882.2004
• Almirón, M., Link, A. J., Furlong, D., & Kolter, R. (1992). A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes & development, 6(12B), 2646–2654. https://doi.org/10.1101/gad.6.12b.2646
• Anderson, G. G., Palermo, J. J., Schilling, J. D., Roth, R., Heuser, J., & Hultgren, S. J. (2003). Intracellular bacterial biofilm-like pods in urinary tract infections. Science (New York, N.Y.), 301(5629), 105–107. https://doi.org/10.1126/science.1084550
• Atlas, R.M., Bartha, R. (1998), Microbial ecology: fundamentals and applications, 4th ed., Addison Wesley Longman California, ISBN: 0805306552.
• Bailey, J.E., Ollis, D.F. (1986). Biochemical engineering fundamentals, 2nd ed. McGraw-Hill, New York, ISBN: 9781138748071.
• Beck, C. M., Willett, J. L., Cunningham, D. A., Kim, J. J., Low, D. A., & Hayes, C. S. (2016). CdiA Effectors from Uropathogenic Escherichia coli Use Heterotrimeric Osmoporins as Receptors to Recognize Target Bacteria. PLoS pathogens, 12(10), e1005925. https://doi.org/10.1371/journal.ppat.1005925
• Bermúdez-Humarán, L. G., Kharrat, P., Chatel, J. M., & Langella, P. (2011). Lactococci and lactobacilli as mucosal delivery vectors for therapeutic proteins and DNA vaccines. Microbial cell factories, 10 Suppl 1(Suppl 1), S4. https://doi.org/10.1186/1475-2859-10-S1-S4
• Chai, T. J., & Foulds, J. (1977). Purification of protein A, an outer membrane component missing in Escherichia coli K-12 ompA mutants. Biochimica et biophysica acta, 493(1), 210–215. https://doi.org/10.1016/0005-2795(77)90274-4
• Chao, L., & Levin, B. R. (1981). Structured habitats and the evolution of anticompetitor toxins in bacteria. Proceedings of the National Academy of Sciences of the United States of America, 78(10), 6324–6328. https://doi.org/10.1073/pnas.78.10.6324
• Choi, U., & Lee, C. R. (2019). Distinct Roles of Outer Membrane Porins in Antibiotic Resistance and Membrane Integrity in Escherichia coli. Frontiers in microbiology, 10, 953. https://doi.org/10.3389/fmicb.2019.00953
• Chaturvedi, D., & Mahalakshmi, R. (2017). Transmembrane β-barrels: Evolution, folding and energetics. Biochimica et biophysica acta. Biomembranes, 1859(12), 2467–2482. https://doi.org/10.1016/j.bbamem.2017.09.020
• Choudhury, D., Thompson, A., Stojanoff, V., Langermann, S., Pinkner, J., Hultgren, S. J., & Knight, S. D. (1999). X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science (New York, N.Y.), 285(5430), 1061–1066. https://doi.org/10.1126/science.285.5430.1061
• Cottet, S., Corthésy-Theulaz, I., Spertini, F., & Corthésy, B. (2002). Microaerophilic conditions permit to mimic in vitro events occurring during in vivo Helicobacter pylori infection and to identify Rho/Ras-associated proteins in cellular signaling. The Journal of biological chemistry, 277(37), 33978–33986. https://doi.org/10.1074/jbc.M201726200
• da Silva, G. P., Mack, M., & Contiero, J. (2009). Glycerol: a promising and abundant carbon source for industrial microbiology. Biotechnology advances, 27(1), 30–39. https://doi.org/10.1016/j.biotechadv.2008.07.006
• Dam, S., Pagès, J. M., & Masi, M. (2017). Dual Regulation of the Small RNA MicC and the Quiescent Porin OmpN in Response to Antibiotic Stress in Escherichia coli. Antibiotics (Basel, Switzerland), 6(4), 33. https://doi.org/10.3390/antibiotics6040033
• Dekoninck, K., Létoquart, J., Laguri, C., Demange, P., Bevernaegie, R., Simorre, J. P., Dehu, O., Iorga, B. I., Elias, B., Cho, S. H., & Collet, J. F. (2020). Defining the function of OmpA in the Rcs stress response. eLife, 9, e60861. https://doi.org/10.7554/eLife.60861
• Diggle, S. P., Griffin, A. S., Campbell, G. S., & West, S. A. (2007). Cooperation and conflict in quorum-sensing bacterial populations. Nature, 450(7168), 411–414. https://doi.org/10.1038/nature06279
• Diner, E. J., Beck, C. M., Webb, J. S., Low, D. A., & Hayes, C. S. (2012). Identification of a target cell permissive factor required for contact-dependent growth inhibition (CDI). Genes & development, 26(5), 515–525. https://doi.org/10.1101/gad.182345.111
• Dupont, M., James, C. E., Chevalier, J., & Pagès, J. M. (2007). An early response to environmental stress involves regulation of OmpX and OmpF, two enterobacterial outer membrane pore-forming proteins. Antimicrobial agents and chemotherapy, 51(9), 3190–3198. https://doi.org/10.1128/AAC.01481-06
• Edwards, R., Baker, H., Whittaker, M. et al. Crystal structure of Escherichia coli manganese superoxide dismutase at 2.1-Å resolution. JBIC 3, 161–171 (1998). https://doi.org/10.1007/s007750050217
• Egli, T., Lendenmann, U., & Snozzi, M. (1993). Kinetics of microbial growth with mixtures of carbon sources. Antonie van Leeuwenhoek, 63(3-4), 289–298. https://doi.org/10.1007/BF00871224
• Ferenci T. (1996). Adaptation to life at micromolar nutrient levels: the regulation of Escherichia coli glucose transport by endoinduction and cAMP. FEMS microbiology reviews, 18(4), 301–317. https://doi.org/10.1111/j.1574-6976.1996.tb00246.x Foulds, J., & Chai, T. J. (1978). New major outer membrane proteins found in an Escherichia coli tolF mutant resistant to bacteriophage TuIb. Journal of bacteriology, 133(3), 1478–1483. https://doi.org/10.1128/jb.133.3.1478-1483.1978
• Fuqua, C., & Greenberg, E. P. (2002). Listening in on bacteria: acyl-homoserine lactone signalling. Nature reviews. Molecular cell biology, 3(9), 685–695. https://doi.org/10.1038/nrm907
• Ghai, I., Bajaj, H., Arun Bafna, J., El Damrany Hussein, H. A., Winterhalter, M., & Wagner, R. (2018). Ampicillin permeation across OmpF, the major outer-membrane channel in Escherichia coli. The Journal of biological chemistry, 293(18), 7030–7037. https://doi.org/10.1074/jbc.RA117.000705
• Ghoul, M., & Mitri, S. (2016). The Ecology and Evolution of Microbial Competition. Trends in microbiology, 24(10), 833–845. https://doi.org/10.1016/j.tim.2016.06.011
• Goers, L., Freemont, P., & Polizzi, K. M. (2014). Co-culture systems and technologies: taking synthetic biology to the next level. Journal of the Royal Society, Interface, 11(96), 20140065. https://doi.org/10.1098/rsif.2014.0065
• Gonzalez, C. F., Ackerley, D. F., Lynch, S. V., & Matin, A. (2005). ChrR, a soluble quinone reductase of Pseudomonas putida that defends against H2O2. The Journal of biological chemistry, 280(24), 22590–22595. https://doi.org/10.1074/jbc.M501654200
• González-Pérez, M. M., van Dillewijn, P., Wittich, R. M., & Ramos, J. L. (2007). Escherichia coli has multiple enzymes that attack TNT and release nitrogen for growth. Environmental microbiology, 9(6), 1535–1540. https://doi.org/10.1111/j.1462-2920.2007.01272.x
• Gonzalez, R., Murarka, A., Dharmadi, Y., & Yazdani, S. S. (2008). A new model for the anaerobic fermentation of glycerol in enteric bacteria: trunk and auxiliary pathways in Escherichia coli. Metabolic engineering, 10(5), 234–245. https://doi.org/10.1016/j.ymben.2008.05.001
• Griffin, A. S., West, S. A., & Buckling, A. (2004). Cooperation and competition in pathogenic bacteria. Nature, 430(7003), 1024–1027. https://doi.org/10.1038/nature02744
• Heffernan, E. J., Wu, L., Louie, J., Okamoto, S., Fierer, J., & Guiney, D. G. (1994). Specificity of the complement resistance and cell association phenotypes encoded by the outer membrane protein genes rck from Salmonella typhimurium and ail from Yersinia enterocolitica. Infection and immunity, 62(11), 5183–5186. https://doi.org/10.1128/iai.62.11.5183-5186.1994
• Hua, Q., Yang, C., Oshima, T., Mori, H., & Shimizu, K. (2004). Analysis of gene expression in Escherichia coli in response to changes of growth-limiting nutrient in chemostat cultures. Applied and environmental microbiology, 70(4), 2354–2366. https://doi.org/10.1128/AEM.70.4.2354-2366.2004
• Kim, W., Racimo, F., Schluter, J., Levy, S. B., & Foster, K. R. (2014). Importance of positioning for microbial evolution. Proceedings of the National Academy of Sciences of the United States of America, 111(16), E1639–E1647. https://doi.org/10.1073/pnas.1323632111
• Klemm, P., Christiansen, G., Kreft, B., Marre, R., & Bergmans, H. (1994). Reciprocal exchange of minor components of type 1 and F1C fimbriae results in hybrid organelles with changed receptor specificities. Journal of bacteriology, 176(8), 2227–2234. https://doi.org/10.1128/jb.176.8.2227-2234.1994
• Klemm, P., Jørgensen, B. J., Kreft, B., & Christiansen, G. (1995). The export systems of type 1 and F1C fimbriae are interchangeable but work in parental pairs. Journal of bacteriology, 177(3), 621–627. https://doi.org/10.1128/jb.177.3.621-627.1995
• Laubacher, M. E., & Ades, S. E. (2008). The Rcs phosphorelay is a cell envelope stress response activated by peptidoglycan stress and contributes to intrinsic antibiotic resistance. Journal of bacteriology, 190(6), 2065–2074. https://doi.org/10.1128/JB.01740-07
• Levina, N., Tötemeyer, S., Stokes, N. R., Louis, P., Jones, M. A., & Booth, I. R. (1999). Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. The EMBO journal, 18(7), 1730–1737. https://doi.org/10.1093/emboj/18.7.1730
• Linton, K. J., & Higgins, C. F. (1998). The Escherichia coli ATP-binding cassette (ABC) proteins. Molecular microbiology, 28(1), 5–13. https://doi.org/10.1046/j.1365-2958.1998.00764.x
• Matin, A. (1979) Microbial regulatory mechanisms at low nutrient concentrations as studied in chemostat, Strategies of microbial life in extreme environments: report of the dahlem workshop on strategy of life in extreme environments, In: Shilo, M. (ed.) Weinheim: Verlag Chemie, 323–339.
• McCord J. M. (1993). Oxygen-derived free radicals. New horizons (Baltimore, Md.), 1(1), 70–76.
• Moraes, C., Mehta, G., Lesher-Perez, S. C., & Takayama, S. (2012). Organs-on-a-chip: a focus on compartmentalized microdevices. Annals of biomedical engineering, 40(6), 1211–1227. https://doi.org/10.1007/s10439-011-0455-6
• Moriarty, D.J.W. (1993) Bacterial growth and starvation in aquatic environments, Starvation in Bacteria, In: Kjelleberg, S. (ed.), Chapter 2, Plenum Press, New York, 25–53.
• Morita, R.Y. (1993) Bioavailability of energy and the starvation state, Starvation in Bacteria, In: Kjelleberg, S. (ed.), Chapter 1, Plenum Press, New York 1-23
• Nai, C., & Meyer, V. (2018). From Axenic to Mixed Cultures: Technological Advances Accelerating a Paradigm Shift in Microbiology. Trends in microbiology, 26(6), 538–554. https://doi.org/10.1016/j.tim.2017.11.004
• Nair, S., & Finkel, S. E. (2004). Dps protects cells against multiple stresses during stationary phase. Journal of bacteriology, 186(13), 4192–4198. https://doi.org/10.1128/JB.186.13.4192-4198.2004
• Notley-McRobb, L., & Ferenci, T. (1999). Adaptive mgl-regulatory mutations and genetic diversity evolving in glucose-limited Escherichia coli populations. Environmental microbiology, 1(1), 33–43. https://doi.org/10.1046/j.1462-2920.1999.00002.x
• Park, J., Kerner, A., Burns, M. A., & Lin, X. N. (2011). Microdroplet-enabled highly parallel co-cultivation of microbial communities. PloS one, 6(2), e17019. https://doi.org/10.1371/journal.pone.0017019
• Rendueles, O., & Ghigo, J. M. (2012). Multi-species biofilms: how to avoid unfriendly neighbors. FEMS microbiology reviews, 36(5), 972–989. https://doi.org/10.1111/j.1574-6976.2012.00328.x
• Riley, M. A., & Gordon, D. M. (1999). The ecological role of bacteriocins in bacterial competition. Trends in microbiology, 7(3), 129–133. https://doi.org/10.1016/s0966-842x(99)01459-6
• Robins, K. J., Hooks, D. O., Rehm, B. H., & Ackerley, D. F. (2013). Escherichia coli NemA is an efficient chromate reductase that can be biologically immobilized to provide a cell free system for remediation of hexavalent chromium. PloS one, 8(3), e59200. https://doi.org/10.1371/journal.pone.0059200
• Rollauer, S. E., Sooreshjani, M. A., Noinaj, N., & Buchanan, S. K. (2015). Outer membrane protein biogenesis in Gram-negative bacteria. Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 370(1679), 20150023. https://doi.org/10.1098/rstb.2015.0023
• Samsudin, F., Boags, A., Piggot, T. J., & Khalid, S. (2017). Braun's Lipoprotein Facilitates OmpA Interaction with the Escherichia coli Cell Wall. Biophysical journal, 113(7), 1496–1504. https://doi.org/10.1016/j.bpj.2017.08.011
• Scholz, R. L., & Greenberg, E. P. (2015). Sociality in Escherichia coli: Enterochelin Is a Private Good at Low Cell Density and Can Be Shared at High Cell Density. Journal of bacteriology, 197(13), 2122–2128. https://doi.org/10.1128/JB.02596-14
• Waters, C. M., & Bassler, B. L. (2005). Quorum sensing: cell-to-cell communication in bacteria. Annual review of cell and developmental biology, 21, 319–346. https://doi.org/10.1146/annurev.cellbio.21.012704.131001
• Wessel, D., Flügge, U.I. (1984). A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids, Analytical Biochemistry, 138, 141-143. DOI: 10.1016/0003-2697(84)90782-6. PMID: 6731838.
• Wick, L. M., Quadroni, M., & Egli, T. (2001). Short- and long-term changes in proteome composition and kinetic properties in a culture of Escherichia coli during transition from glucose-excess to glucose-limited growth conditions in continuous culture and vice versa. Environmental microbiology, 3(9), 588–599. https://doi.org/10.1046/j.1462-2920.2001.00231.x
• Zhu, F., Chen, G., Wu, J., & Pan, J. (2013). Structure revision and cytotoxic activity of marinamide and its methyl ester, novel alkaloids produced by co-cultures of two marine-derived mangrove endophytic fungi. Natural product research, 27(21), 1960–1964. https://doi.org/10.1080/14786419.2013.800980