Intact cell MALDI-TOF mass spectrometric analysis of Chroococcidiopsis cyanobacteria for classification purposes and identification of possible marker proteins

. 2018 ; 13 (11) : e0208275. [epub] 20181129

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid30496311

Cyanobacteria represent a bacterial phyllum characteristic by the ability to photosynthesize. They are potentially applicable for the production of useful compounds but may also cause poisoning or at least health problems as they can produce cyanotoxins. The introduction of a fast methodology is important not only for fundamental taxonomic purposes, but also for reliable identifications in biological studies. In this work, we have used matrix-assisted laser desorption/ionization time-of-flight mass spectrometry of intact cells to study Chroococcidiopsis strains. A library of the obtained reference mass spectra containing characteristic peptide/protein profiles was examined by software tools to characterize similarities and differences applicable for diagnostics and taxonomy. Both a similarity tree and heat map constructed from the mass spectrometric data proved consistent with 16S rRNA sequencing results. We show as novelty that a binary matrix combining ferulic and sinapinic acids performs well in acquiring reproducible mass spectra of cyanobacteria. Using the matrix solvent, a protein extraction from cells was done. After polyacrylamide gel electrophoresis, the separated protein fractions were in-gel digested and the resulting peptides analyzed by liquid chromatography coupled with tandem mass spectrometry. For the first time, photosystem protein components, phycobilisome proteins, electron transport proteins, nitrogen-metabolism and nucleic acids binding-proteins, cytochromes plus other enzymes and various uncharacterized proteins could be assigned to characteristic peaks in the mass spectrometric profiles and some of them suggested as markers in addition to 30S and 50S ribosomal proteins known from previous studies employing intact cell mass spectrometry of microorganisms.

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Knoll AH. Cyanobacteria and earth history In: Herrero A, Flores E, editors. The cyanobacteria: molecular biology, genomics and evolution. Norfolk: Caister Academic Press; 2008. p. 1–19.

Geitler L. Cyanophyceae von Europa unter Berücksichtigung der anderen Kontinente In: Kolkwitz R, editor. Dr. L. Rabenhorst’s Kryptogamen—Flora von Deutschland, Österreich und der Schweiz, Vol. XIV Leipzig: Akademische Verlagsgesellschaft; 1932. p. 1–1196. German.

Stanier RY, Sistrom WR, Hansen TA, Whitton BA, Castenholz RW, Pfennig N, et al. Proposal to place the nomenclature of the cyanobacteria (blue-green algae) under the rules of the International Code of Nomenclature of Bacteria. Int J Syst Bacteriol. 1978;28(2):335–6; 10.1099/00207713-28-2-335 DOI

Anagnostidis K, Komárek J. Modern approach to the classification system of cyanophytes. 1-Introduction. Arch Hydrobiol Suppl Algol Stud. 1985;38–39:291–302.

Komárek J, Kaštovský J, Mareš J, Johansen JR. Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia. 2014;86(4):295–335.

Dvořák P, Hindák F, Hašler P, Hindáková A, Poulíčková A. Morphological and molecular studies of Neosynechococcus sphagnicola gen. et sp. nov. (Cyanobacteria, Synechococcales). Phytotaxa 2014;170(1):24–34; 10.11646/phytotaxa.170.1.3 DOI

Nagy E, Becker S, Kostrzewa M, Barta N, Urbán E. The value of MALDI-TOF MS for the identification of clinically relevant anaerobic bacteria in routine laboratories. J Med Microbiol. 2012;61(10):1393–400; 10.1099/jmm.0.043927-0 PubMed DOI

Chalupová J, Raus M, Sedlářová M, Šebela M. Identification of fungal microorganisms by MALDI-TOF mass spectrometry. Biotechnol Adv. 2014;32(1):230–41; 10.1016/j.biotechadv.2013.11.002 PubMed DOI

Singhal N, Kumar M, Kanaujia PK, Virdi JS. MALDI-TOF mass spectrometry: an emerging technology for microbial identification and diagnosis. Front Microbiol. 2015;6:791; 10.3389/fmicb.2015.00791 PubMed DOI PMC

Singhal N, Kumar M, Virdi JS. MALDI-TOF MS in clinical parasitology: applications, constraints and prospects. Parasitology. 2016;143(12):1491–500; 10.1017/S0031182016001189 PubMed DOI

Beinhauer J, Raus M, Hanzalová A, Horčička P, Šebela M. Intact spore MALDI-TOF mass spectrometry and proteomic analysis of Puccinia pathogenic fungi. Biochim Biophys Acta. 2016;1864(9):1093–103; 10.1016/j.bbapap.2016.06.002 PubMed DOI

Šedo O, Sedláček I, Zdráhal Z. Sample preparation methods for MALDI-MS profiling of bacteria. Mass Spectrom Rev. 2011;30(3):417–34; 10.1002/mas.20287 PubMed DOI

Erhard M, von Döhren H, Jungblut P. Rapid typing and elucidation of new secondary metabolites of intact cyanobacteria using MALDI-TOF mass spectrometry. Nat Biotechnol. 1997; 15:906–9; 10.1038/nbt0997-906 PubMed DOI

Fastner J, Erhard M, von Döhren H. Determination of oligopeptide diversity within a natural population of Microcystis spp. (cyanobacteria) by typing single colonies by matrix-assisted laser desorption ionization–time of flight mass spectrometry. Appl Environ Microbiol. 2001;67(11):5069–76. 10.1128/AEM.67.11.5069-5076.2001 PubMed DOI PMC

Sun LW, Jiang WJ, Sato H, Kawachi M, Lu XW. Rapid classification and identification of Microcystis aeruginosa strains using MALDI-TOF MS and polygenetic analysis. PLOS One. 2016;11(5): e0156275; 10.1371/journal.pone.0156275 PubMed DOI PMC

Imanishi SY, Nakayama T, Asukabe H, Harada K. Application of MALDI Biotyper to cyanobacterial profiling. Rapid Commun Mass Spectrom.2017; 31(4):325–32; 10.1002/rcm.7793 PubMed DOI

Staub R. 1961. Ernährungphysiologish-autökologische Untersuchung an den planktonischen Blaualge Oscillatoria rubescens DC. Schweiz Z Hydrol. 1961;23(1):82–198. German; 10.3929/ethz-a-000092335 DOI

Raus M, Šebela M. BIOSPEAN: a freeware tool for processing spectra from MALDI intact cell/spore mass spectrometry. J Proteomics Bioinform. 2013; 6(12):283–7; 10.4172/jpb.1000292 DOI

Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(5259):680–5; 10.1038/227680a0 PubMed DOI

Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc. 2006;1(6):2856–60; 10.1038/nprot.2006.468 PubMed DOI

Šebela M, Štosová T, Havliš J, Wielsch N, Thomas H, Zdráhal Z, et al. Thermostable trypsin conjugates for high-throughput proteomics: synthesis and performance evaluation. Proteomics. 2006;6(10):2959–63; 10.1002/pmic.200500576 PubMed DOI

Petrovská B, Jeřábková H, Chamrád I, Vrána J, Lenobel R, Uřinovská J, et al. Proteomic analysis of barley cell nuclei purified by flow sorting. Cytogenet Genome Res. 2014;143(1–3):78–86; 10.1159/000365311 PubMed DOI

Boyer SL, Johansen JR, Flechtner VR, Howard GL. Phylogeny and genetic variance in terrestrial Microcoleus (Cyanophyceae) species based on sequence analysis of the 16s rRNA gene and associated 16S-23S ITS region. J Phycol. 2002;38(6):1222–35; 10.1046/j.1529-8817.2002.01168.x DOI

Dvořák P, Hašler P, Poulíčková A. Phylogeography of the Microcoleus vaginatus (cyanobacteria) from three continents–a spatial and temporal characterization. PLoS ONE. 2012;7(6):e40153; 10.1371/journal.pone.0040153 PubMed DOI PMC

Boyer SL, Flechtner VR, Johansen JR. Is the 16S-23S rRNA internal transcribed spacer region a good tool for use in molecular systematics and population genetics? A case study in cyanobacteria. Mol Biol Evol. 2001;18(6):1057–69; 10.1093/oxfordjournals.molbev.a003877 PubMed DOI

Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30(14):3059–66. PubMed PMC

Posada D. 2008. jModelTest: phylogenetic model averaging. Mol Biol Evol. 2008;25(7):1253–6; 10.1093/molbev/msn083 PubMed DOI

Ronquist F, Huelsenbeck JP. Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19(12):1572–4; 10.1093/bioinformatics/btg180 PubMed DOI

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312–3; 10.1093/bioinformatics/btu033 PubMed DOI PMC

Havlíček V, Lemr K, Schug KA. Current trends in microbial diagnostics based on mass spectrometry. Anal Chem. 2012;85(2):790−7; 10.1021/ac3031866 PubMed DOI

Chalupová J, Sedlářová M, Helmel M, Řehulka P, Marchetti-Deschmann M, Allmaier G, et al. MALDI-based intact spore mass spectrometry of downy and powdery mildews. J Mass Spectrom. 2012;47(8):978–86; 10.1002/jms.3046 PubMed DOI

Ziegler D, Pothier JF, Ardley J, Fossou RK, Pflüger V, de Meyer S, et al. Ribosomal protein biomarkers provide root nodule bacterial identification by MALDI-TOF MS. Appl Microbiol Biotechnol. 2015;99(13):5547–62; 10.1007/s00253-015-6515-3 PubMed DOI

Sauget M, Valot B, Bertrand X, Hocquet D. Can MALDI-TOF mass spectrometry reasonably type bacteria? Trends Microbiol. 2017;25(6):447–55; 10.1016/j.tim.2016.12.006 PubMed DOI

Hillenkamp F, Jaskolla TW, Karas M. The MALDI process and method In: Hillenkamp F, Peter-Katalinic J, editors. MALDI MS: a practical guide to instrumentation, methods and applications. Weinheim: Wiley-VCH Verlag; 2007. p. 1–28.

Beavis RC, Chait BT. Cinnamic acid derivatives as matrices for ultraviolet laser desorption mass spectrometry of proteins. Rapid Commun Mass Spectrom. 1989;3(12):432–5; 10.1002/rcm.1290031207 PubMed DOI

Nilsson CL. Fingerprinting of Helicobacter pylori strains by matrix-assisted laser desorption/ionization mass spectrometric analysis. Rapid Commun Mass Spectrom. 1999;13(11):1067–71; 10.1002/(SICI)1097-0231(19990615)13:11<1067::AID-RCM612>3.0.CO;2-N PubMed DOI

Amiri-Eliasi B, Fenselau C. Characterization of protein biomarkers desorbed by MALDI from whole fungal cells. Anal Chem. 2001;73(21):5228–31; 10.1021/ac010651t PubMed DOI

Fenselau C, Demirev PA. Characterization of intact microorganisms by MALDI mass spectrometry. Mass Spectrom Rev. 2001;20(4):157–71; 10.1002/mas.10004 PubMed DOI

Liyanage R, Lay JO Jr. An introduction to MALDI-TOF MS In: Wilkins CL, Lay JO, editors. Identification of microorganisms by mass spectrometry. Hoboken, NJ: John Wiley & Sons; 2006. pp. 39–60.

Kemptner J, Marchetti-Deschmann M, Kubicek CP, Allmaier G. Mixed volume sample preparation method for intact cell mass spectrometry of Fusarium spores. J Mass Spectrom. 2009;44(11):1622–4; 10.1002/jms.1669 PubMed DOI

Liu Z, Schey KL. Optimization of a MALDI TOF-TOF mass spectrometer for intact protein analysis. J Am Soc Mass Spectrom. 2005;16(4): 482–90; 10.1016/j.jasms.2004.12.018 PubMed DOI

DeRuyter YS, Fromme P. Molecular structure of the photosynthetic apparatus In: Herrero A, Flores E, editors. Norfolk: Caister Academic Press; 2008. p. 217–270.

Fiore MF, Sant’Anna CL, de Paiva Azevedo MT, Komárek J, Kaštovský J, Sulek J, et al. The cyanobacterial genus Brasilonema, gen. nov., a molecular and phenotypic evaluation. J Phycol. 2007;43(4):789–98; 10.1111/j.1529-8817.2007.00376.x DOI

Hašler P, Dvořák P, Johansen JR, Kitner M, Ondřej V, Poulíčková A. Morphological and molecular study of epipelic filamentous genera Phormidium, Microcoleus and Geitlerinema (Oscillatoriales, Cyanophyta/Cyanobacteria). Fottea. 2012;12(2):341–56; 10.5507/fot.2012.024 DOI

Hašler P, Casamatta DA, Dvořák P, Poulíčková A. Jacksonvillea apiculata (Oscillatoriales, Cyanobacteria) gen. & sp. nov.: a new genus of filamentous, epipsamic cyanobacteria from North Florida. Phycologia. 2017;56(3):284–95; 10.2216/16.62.1 DOI

Fewer D, Friedl T, Büdel B. Chroococcidiopsis and heterocyst-differentiating cyanobacteria are each other´s closest living relatives. Mol Phylogenet Evol. 2002;23(1):82–90; 10.1006/mpev.2001.1075 PubMed DOI

Donner A. The case of Chroococcidiopsis: New phylogenetic and morphological insights into ecologically important cyanobacteria [dissertation] Technische Universität Kaiserslautern; 2013.

De Los Ríos A, Grube M, Sancho LG, Ascaso C. Ultrastructural and genetic characteristics of endolithic cyanobacterial biofilms colonizing Antarctic granite rocks. FEMS Microbiol Ecol. 2006;59(2):386–95; 10.1111/j.1574-6941.2006.00256.x PubMed DOI

Sauer S, Kliem M. Mass spectrometry tools for the classification and identification of bacteria. Nat Rev Microbiol. 2010;8:74–82; 10.1038/nrmicro2243 PubMed DOI

Geitler L. Diagnosen neuer Blaualgen von den Sunda-Inseln In: Thienemann A, editor. Archiv Für Hydrobiologie, Supplement-Band XII. E. Stuttgart: Schweizerbart´sche Verlagsbuchhandlung; 1934. p. 622–634. German.

Tsai CS. Biomacromolecules: Introduction to structure, function and informatics Hoboken, NJ: John Wiley & Sons; 2007. p. 594–595.

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