The Influence of Metabolic Inhibitors, Antibiotics, and Microgravity on Intact Cell MALDI-TOF Mass Spectra of the Cyanobacterium Synechococcus Sp. UPOC S4

. 2021 Mar 17 ; 26 (6) : . [epub] 20210317

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33802864

Grantová podpora
IGA_PrF_2019_022 Univerzita Palackého v Olomouci

The aim and novelty of this paper are found in assessing the influence of inhibitors and antibiotics on intact cell MALDI-TOF mass spectra of the cyanobacterium Synechococcus sp. UPOC S4 and to check the impact on reliability of identification. Defining the limits of this method is important for its use in biology and applied science. The compounds included inhibitors of respiration, glycolysis, citrate cycle, and proteosynthesis. They were used at 1-10 μM concentrations and different periods of up to 3 weeks. Cells were also grown without inhibitors in a microgravity because of expected strong effects. Mass spectra were evaluated using controls and interpreted in terms of differential peaks and their assignment to protein sequences by mass. Antibiotics, azide, and bromopyruvate had the greatest impact. The spectral patterns were markedly altered after a prolonged incubation at higher concentrations, which precluded identification in the database of reference spectra. The incubation in microgravity showed a similar effect. These differences were evident in dendrograms constructed from the spectral data. Enzyme inhibitors affected the spectra to a smaller extent. This study shows that only a long-term presence of antibiotics and strong metabolic inhibitors in the medium at 10-5 M concentrations hinders the correct identification of cyanobacteria by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF).

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Palinska K.A., Surosz W. Taxonomy of cyanobacteria: A contribution to consensus approach. Hydrologia. 2014;740:1–11. doi: 10.1007/s10750-014-1971-9. DOI

Clark A.E., Kaleta E.J., Arora A., Wolk D.M. Matrix-assisted laser desorption ionization–time of flight mass apectrometry: A fundamental shift in the routine practice of clinical microbiology. Clin. Microbiol. Rev. 2013;26:547–603. doi: 10.1128/CMR.00072-12. PubMed DOI PMC

Drissner D., Freimoser F.M. MALDI-TOF mass spectroscopy of yeasts and filamentous fungi for research and diagnostics in the agricultural value chain. Chem. Biol. Technol. Agric. 2017;4:13. doi: 10.1186/s40538-017-0095-7. DOI

Tadros M., Petrich A. Evaluation of MALDI-TOF mass spectrometry and Sepsityper Kit™ for the direct identification of organisms from sterile body fluids in a Canadian pediatric hospital. Can. J. Infect. Dis. Med. Microbiol. 2013;24:191–194. doi: 10.1155/2013/701093. PubMed DOI PMC

Hou T.Y., Chiang-Ni C., Teng S.H. Current status of MALDI-TOF mass spectrometry in clinical microbiology. J. Food Drug Anal. 2019;27:404–414. doi: 10.1016/j.jfda.2019.01.001. PubMed DOI PMC

Ge M.C., Kuo A.J., Liu K.L., Wen Y.H., Chia J.H., Chang P.Y., Lee M.H., Wu T.L., Chang S.C., Lu J.J. Routine identification of microorganisms by matrix-assisted laser desorption ionization time-of-flight mass spectrometry: Success rate, economic analysis, and clinical outcome. J. Microbiol. Immunol. Infect. 2017;50:662–668. doi: 10.1016/j.jmii.2016.06.002. PubMed DOI

Khot P.D., Fisher M.A. Novel approach for differentiating Shigella species and Escherichia coli by matrix-assisted laser desorption ionization–time of flight mass spectrometry. J. Clin. Microbiol. 2013;51:3711–3716. doi: 10.1128/JCM.01526-13. PubMed DOI PMC

Sauget M., Valot B., Bertrand X., Hocquet D. Can MALDI-TOF mass spectrometry reasonably type bacteria? Trends Microbiol. 2017;25:447–455. doi: 10.1016/j.tim.2016.12.006. PubMed DOI

Sun L.W., Jiang W.J., Sato H., Kawachi M., Lu X.W. Rapid classification and identification of Microcystis aeruginosa strains using MALDI–TOF MS and polygenetic analysis. PLoS ONE. 2016;11:e0156275. doi: 10.1371/journal.pone.0156275. PubMed DOI PMC

Šebela M., Jahodářová E., Raus M., Lenobel R., Hašler P. Intact cell MALDI-TOF mass spectrometric analysis of Chroococcidiopsis cyanobacteria for taxonomic purposes and identification of marker proteins. PLoS ONE. 2018;13:e0208275. doi: 10.1371/journal.pone.0208275. PubMed DOI PMC

Peng X., Yang J., Gao Y. Proteomic analyses of changes in Synechococcus sp. PCC7942 following UV-C stress. Photochem. Photobiol. 2017;93:1073–1080. doi: 10.1111/php.12726. PubMed DOI

Hongsthong A., Sirijuntarut M., Prommeenate P., Lertladaluck K., Porkaew K., Cheevadhanarak S., Tanticharoen M. Proteome analysis at the subcellular level of the cyanobacterium Spirulina platensis in response to low-temperature stress conditions. FEMS Microbiol. Lett. 2008;288:92–101. doi: 10.1111/j.1574-6968.2008.01330.x. PubMed DOI

Kurdrid P., Senachak J., Sirijuntarut M., Yutthanasirikul R., Phuengcharoen P., Jeamton W., Roytrakul S., Cheevadhanarak S., Hongsthong A. Comparative analysis of the Spirulina platensis subcellular proteome in response to low-and high-temperature stresses: Uncovering cross-talk of signaling components. Proteome Sci. 2011;9:39. doi: 10.1186/1477-5956-9-39. PubMed DOI PMC

Pandhal J., Ow S.Y., Wright P.C., Biggs C.A. Comparative proteomics study of salt tolerance between a nonsequenced extremely halotolerant cyanobacterium and its mildly halotolerant relative using in vivo metabolic labeling and in vitro isobaric labeling. J. Proteome Res. 2009;8:818–828. doi: 10.1021/pr800283q. PubMed DOI

Yadav R.K., Thagela P., Tripathi K., Abraham G. Physiological and proteomic analysis of salinity tolerance of the halotolerant cyanobacterium Anabaena sp. World J. Microbiol. Biotechnol. 2016;32:147. doi: 10.1007/s11274-016-2098-0. PubMed DOI

Kurian D., Phadwal K., Mäenpää P. Proteomic characterization of acid stress response in Synechocystis sp. PCC 6803. Proteomics. 2006;6:3614–3624. doi: 10.1002/pmic.200600033. PubMed DOI

Zhang L.F., Yang H.M., Cui S.X., Hu J., Wang J., Kuang T.Y., Norling B., Huang F. Proteomic analysis of plasma membranes of cyanobacterium Synechocystis sp. strain PCC 6803 in response to high pH stress. J. Proteome Res. 2009;8:2892–2902. doi: 10.1021/pr900024w. PubMed DOI

Mehta A., López-Maury L., Florencio F.J. Proteomic pattern alterations of the cyanobacterium Synechocystis sp. PCC 6803 in response to cadmium, nickel and cobalt. J. Proteom. 2014;102:98–112. doi: 10.1016/j.jprot.2014.03.002. PubMed DOI

Babele P.K., Kumar J., Chaturvedi V. Proteomic de-regulation in cyanobacteria in response to abiotic stresses. Front. Microbiol. 2019;10:1315. doi: 10.3389/fmicb.2019.01315. PubMed DOI PMC

Singh J.S., Kumar A., Rai A.N., Singh D.P. Cyanobacteria: A precious bio-resource in agriculture, ecosystem, and environmental sustainability. Front. Microbiol. 2016;7:529. doi: 10.3389/fmicb.2016.00529. PubMed DOI PMC

Groendahl S., Fink P. High dietary quality of non-toxic cyanobacteria for a benthic grazer and its implications for the control of cyanobacterial biofilms. BMC Ecol. 2017;17:20. doi: 10.1186/s12898-017-0130-3. PubMed DOI PMC

Quiblier C., Wood S., Echenique-Subiabre I., Heath M., Villeneuve A., Humbert J.F. A review of current knowledge on toxic benthic freshwater cyanobacteria—Ecology, toxin production and risk management. Water Res. 2013;47:5464–5479. doi: 10.1016/j.watres.2013.06.042. PubMed DOI

Asukabe H., Akahori S., Ueno E., Nakayama T., Yamashita R., Arii S., Harada K., Imanishi S.Y. Cyanobacterial classification with the toxicity using MALDI Biotyper. J. Am. Soc. Mass Spectrom. 2020;31:1572–1578. doi: 10.1021/jasms.0c00148. PubMed DOI

Cardaci S., Desideri E., Ciriolo M.R. Targeting aerobic glycolysis: 3-bromopyruvate as a promising anticancer drug. J. Bioenerg. Biomembr. 2012;44:17–29. doi: 10.1007/s10863-012-9422-7. PubMed DOI

Chen Z., Zhang H., Lu W., Huang P. Role of mitochondria-associated hexokinase II in cancer cell death induced by 3-bromopyruvate. Biochim. Biophys. Acta Bioenerg. 2009;1787:553–560. doi: 10.1016/j.bbabio.2009.03.003. PubMed DOI PMC

Ganapathy-Kanniappan S., Geschwind J.F.H., Kunjithapatham R., Buijs M., Vossen J.A., Tchernyshyov I., Cole R.N., Syed L.H., Rao P.R., Ota S., et al. Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) is pyruvylated during 3-bromopyruvate mediated cancer cell death. Anticancer Res. 2009;29:4909–4918. PubMed PMC

Wick A.N., Drury D.R., Nakada H.I., Wolfe J.B. Localization of the primary metabolic block produced by 2-deoxyglucose. J. Biol. Chem. 1957;224:963–969. doi: 10.1016/S0021-9258(18)64988-9. PubMed DOI

Ralser M., Wamelink M.M., Struys E.A., Joppich C., Krobitsch S., Jakobs C., Lehrach H. A catabolic block does not sufficiently explain how 2-deoxy-D-glucose inhibits cell growth. Proc. Natl. Acad. Sci. USA. 2008;105:17807–17811. doi: 10.1073/pnas.0803090105. PubMed DOI PMC

Pajak B., Siwiak E., Sołtyka M., Priebe A., Zieliński R., Fokt I., Ziemniak M., Jaśkiewicz A., Borowski R., Domoradzki T., et al. 2-Deoxy-D-glucose and its analogs: From diagnostic to therapeutic agents. Int. J. Mol. Sci. 2020;21:234. doi: 10.3390/ijms21010234. PubMed DOI PMC

Goncharov N.V., Jenkins R.O., Radilov A.S. Toxicology of fluoroacetate: A review, with possible directions for therapy research. J. App. Toxicol. 2006;26:148–161. doi: 10.1002/jat.1118. PubMed DOI

Lauble H., Kennedy M.C., Emptage M.H., Beinert H., Stout C.D. The reaction of fluorocitrate with aconitase and the crystal structure of the enzyme inhibitor complex. Proc. Natl Acad. Sci. USA. 1996;93:13699–13703. doi: 10.1073/pnas.93.24.13699. PubMed DOI PMC

Potter V.R., Elvehjem C.A. The effect of inhibitors on succinoxidase. J. Biol. Chem. 1937;117:341–349. doi: 10.1016/S0021-9258(18)74609-7. DOI

Kim H., Esser L., Hossain M.B., Xia D., Yu C.A., Rizo-Rey J., van der Helm D., Deisenhofer J. Structure of antimycin A1, a specific electron transfer inhibitor of ubiquinol−cytochrome c oxidoreductase. J. Am. Chem. Soc. 1999;121:4902–4903. doi: 10.1021/ja990190h. DOI

Joët T., Cournac L., Horvath E.M., Medgyesy P., Peltier G. Increased sensitivity of photosynthesis to antimycin A induced by inactivation of the chloroplast ndhB gene. Evidence for a participation of the NADH-dehydrogenase complex to cyclic electron flow around photosystem I. Plant Physiol. 2001;125:1919–1929. doi: 10.1104/pp.125.4.1919. PubMed DOI PMC

Ortiz de Montellano P.R., David S.K., Ator M.A., Tew D. Mechanism-based inactivation of horseradish peroxidase by sodium azide. Formation of meso-azidoprotoporphyrin IX. Biochemistry. 1988;27:5470–5476. doi: 10.1021/bi00415a013. PubMed DOI

Yoshikawa S., Shinzawa-Itoh K., Nakashima R., Yaono R., Yamashita E., Inoue N., Yao M., Fei M.J., Libeu C.P., Mizushima T., et al. Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science. 1998;280:1723–1729. doi: 10.1126/science.280.5370.1723. PubMed DOI

Forti G., Gerola P. Inhibition of photosynthesis by azide and cyanide and the role of oxygen in photosynthesis. Plant Physiol. 1977;59:859–862. doi: 10.1104/pp.59.5.859. PubMed DOI PMC

Balbi H.J. Chloramphenicol: A review. Pediatr. Rev. 2004;25:284–288. doi: 10.1542/pir.25-8-284. PubMed DOI

Luzzatto L., Apirion D., Schlessinger D. Mechanism of action of streptomycin in E. coli: Interruption of the ribosome cycle at the initiation of protein synthesis. Proc. Natl. Acad. Sci. USA. 1968;60:873–880. doi: 10.1073/pnas.60.3.873. PubMed DOI PMC

Demirci H., Murphy F., IV, Murphy E., Gregory S.T., Dahlberg A.E., Jogl G. A structural basis for streptomycin-induced misreading of the genetic code. Nat. Commun. 2013;4:1355. doi: 10.1038/ncomms2346. PubMed DOI PMC

Hoson T., Kamisaka S., Masuda Y., Yamashita M. Changes in plant growth processes under microgravity conditions simulated by a three-dimensional clinostat. Bot. Mag. Tokyo. 1992;105:53–70. doi: 10.1007/BF02489403. DOI

Pietsch J., Bauer J., Egli M., Infanger M., Wise P., Ulbrich C., Grimm D. The effects of weightlessness on the human organism and mammalian cells. Curr. Mol. Med. 2011;11:350–364. doi: 10.2174/156652411795976600. PubMed DOI

Isidori M., Lavorgna M., Nardelli A., Pascarella A., Parrella A. Toxic and genotoxic evaluation of six antibiotics on non-target organisms. Sci. Total Envion. 2005;346:87–98. doi: 10.1016/j.scitotenv.2004.11.017. PubMed DOI

van der Grinten E., Pikkemaat M.G., van den Brandhof E.J., Stroomberg G.J., Kraak M.H.S. Comparing the sensitivity of algal, cyanobacterial and bacterial bioassays to different groups of antibiotics. Chemosphere. 2010;80:1–6. doi: 10.1016/j.chemosphere.2010.04.011. PubMed DOI

González-Pleiter M., Gonzalo S., Rodea-Palomares I., Leganés F., Rosal R., Boltes K., Marco E., Fernández-Piñas F. Toxicity of five antibiotics and their mixtures towards photosynthetic aquatic organisms: Implications for environmental risk assessment. Water Res. 2013;47:2050–2064. doi: 10.1016/j.watres.2013.01.020. PubMed DOI

Qian H., Li J., Pan X., Sun Z., Ye C., Jin G., Fu Z. Effects of streptomycin on growth of algae Chlorella vulgaris and Microcystis aeruginosa. Environ. Toxicol. 2012;27:229–237. doi: 10.1002/tox.20636. PubMed DOI

Brilisauer K., Rapp J., Rath P., Schöllhorn A., Bleul L., Weiss E., Stahl M., Grond S., Forchhammer K. Cyanobacterial antimetabolite 7-deoxy-sedoheptulose blocks the shikimate pathway to inhibit the growth of prototrophic organisms. Nat. Commun. 2019;10:545. doi: 10.1038/s41467-019-08476-8. PubMed DOI PMC

Gallon J.R., Ul-Haque M.I., Chaplin A.E. Fluoroacetate metabolism in Gloeocapsa sp. LB795 and its relationship to acetylene reduction (nitrogen fixation) J. Gen. Microbiol. 1978;106:329–336. doi: 10.1099/00221287-106-2-329. DOI

Visca P., Pisa F., Imperi F. The antimetabolite 3-bromopyruvate selectively inhibits Staphylococcus aureus. Int. J. Antimicrob. Agents. 2019;53:449–455. doi: 10.1016/j.ijantimicag.2018.11.008. PubMed DOI

Lichstein H.C., Soule M.H. Studies of the effect of sodium azide on microbic growth and respiration I. The action of sodium azide on microbic growth. J. Bacteriol. 1944;47:221–230. doi: 10.1128/JB.47.3.221-230.1944. PubMed DOI PMC

Oliver D.B., Cabelli R.J., Dolan K.M., Jarosik G.P. Azide-resistant mutants of Escherichia coli alter the SecA protein, an azide-sensitive component of the protein export machinery. Proc. Natl. Acad. Sci. USA. 1990;87:8227–8231. doi: 10.1073/pnas.87.21.8227. PubMed DOI PMC

Hickey C.W., Blaise C., Costan G. Microtesting appraisal of ATP and cell recovery toxicity end points after acute exposure of Selenastrum capricornutum to selected chemicals. Environ. Toxicol. Water Qual. 1991;6:383–403. doi: 10.1002/tox.2530060404. DOI

Hoiczyk E., Hansel A. Cyanobacterial cell walls: News from an unusual prokaryotic envelope. J. Bacteriol. 2000;182:1191–1199. doi: 10.1128/JB.182.5.1191-1199.2000. PubMed DOI PMC

Amiri-Eliasi B., Fenselau C. Characterization of protein biomarkers desorbed by MALDI from whole fungal cells. Anal. Chem. 2001;73:5228–5231. doi: 10.1021/ac010651t. PubMed DOI

Komenda J., Sobotka R. Cyanobacterial high-light-inducible proteins—Protectors of chlorophyll–protein synthesis and assembly. Biochim. Biophys. Acta Bioenerg. 2016;1875:288–295. doi: 10.1016/j.bbabio.2015.08.011. PubMed DOI

Fei Q., Gao E.B., Liu B., Wei Y., Ning D. A toxin-antitoxin system VapBC15 from Synechocystis sp. PCC 6803 shows distinct regulatory features. Genes. 2018;9:173. doi: 10.3390/genes9040173. PubMed DOI PMC

Staub R. Ernährungphysiologish-autökologische Untersuchung an den planktonischen Blaualge Oscillatoria rubescens DC. Schweiz. Z. Hydrol. 1961;23:82–198.

Raus M., Šebela M. BIOSPEAN: A freeware tool for processing spectra from MALDI intact cell/spore mass spectrometry. J. Proteom. Bioinform. 2013;6:283–287. doi: 10.4172/jpb.1000292. DOI

Strohalm M., Hassman M., Košata B., Kodíček M. mMass data miner: An open source alternative for mass spectrometric data analysis. Rapid Commun. Mass Spec. 2008;22:905–908. doi: 10.1002/rcm.3444. PubMed DOI

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