Фунгистатическая активность штаммов Serratia proteamaculans и S. liquefaciens, выделенных в Греции из отложений гуано летучих мышей в подземной пещере
Автор: Майкл Г., Рейзопулос А., Вагелас Х.
Журнал: Сельскохозяйственная биология @agrobiology
Рубрика: Сельскохозяйственная микробиология
Статья в выпуске: 3 т.57, 2022 года.
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Представители рода Serratia вызывают повышенный научный интерес, поскольку они распространены практически повсеместно и проявляют эмульгирующие, поверхностно-активные, противообрастающие, противоопухолевые и противомикробные свойства. Вода - естественная среда обитания для нескольких видов серраций. В представляемой публикации мы сообщаем о первом выделении S. proteamaculans из гуано летучих мышей. Цель нашей работы заключалась в изучении гуано летучих мышей из подземной водной экосистемы на наличие изолятов Serratia , активных против фитопатогенных грибов. Штаммы Serratia , которые выделили из отложений гуано в пещере в регионе Фессалия (Эолия, Греция), первоначально были обозначены как Sl2 и Sl4, оказались способны ферментировать D-глюкозу, другие углеводы (D-маннит, D-маннозу) и сахарозу в качестве источников углерода и сахаров. Для обоих штаммов оптимальная температура для роста - 28 °С, при этом штамм Sl4 способен расти и при 4 °С. Штаммы бактерий Sl2 и Sl4 были отнесены к группе Serratia liquefaciens с помощью автоматического бактериологического анализатора VITEK® 2 («bioMerieux SA», Франция) и точно идентифицированы до вида с использованием MALDI-TOF MS («bioMerieux SA», Франция). MALDI-TOF MS классифицировала штамм Sl2 как S. proteamaculans , а штамм Sl4 - как S. liquefaciens . Насколько нам известно, это первое в мировой научной литературе сообщение о выделении и классификации S. proteamaculans из гуано летучих мышей. При 28 °С оба изученных штамма Serratia продуцировали продигиозин, при этом его оптимальную продукцию отмечали через 72 ч инкубации. Определение активности штаммов S. liquefaciens и S. proteamaculans против фитопатогенных грибов ( Fusarium oxysporum , Alternaria alternata , Botrytis cinerea , Sclerotinia sclerotiorum и Rhizoctonia solani ) in vitro показало способность изученных серраций продуцировать свободно диффундирующие соединения с фунгистатической активностью in vitro. Это первое сообщение о том, что штаммы S. liquefaciens и S. proteamaculans , выделенные из гуано летучих мышей, потенциально могут рассматриваться как биоагенты против фитопатогенных грибов. Исследование взаимодействия между фитопатогенными грибами и бактериями S. liquefaciens и S. proteamaculans подтвердили их эффективность для биоконтроля этих грибных патогенов.
Serratia spp, гуано летучих мышей, подземная водная среда, вторичные метаболиты, биоконтроль
Короткий адрес: https://sciup.org/142236371
IDR: 142236371 | DOI: 10.15389/agrobiology.2022.3.566rus
Список литературы Фунгистатическая активность штаммов Serratia proteamaculans и S. liquefaciens, выделенных в Греции из отложений гуано летучих мышей в подземной пещере
- García-Fraile P., Chudícková M., Benada O., Pikula J., Kolarík M. Serratia myotis sp. nov. and Serratia vespertilionis sp. nov., isolated from bats hibernating in caves. International Journal of Systematic and Evolutionary Microbiology, 2015, 65(Pt_1): 90-94 (doi: 10.1099/ijs.0.066407-0).
- Grimont F., Grimont P.A.D. The genus Serratia. In: The prokaryotes: a handbook on the biology of bacteria, 3rd edn. /M. Dworkin, S. Falkow, E. Rosenberg, K.H. Schleifer, E. Stackebrandt (eds.). New York, Springer, 2006: 219-244 (doi: 10.1007/0-387-30746-X_11).
- Grimont F., Grimont P.A.D. Genus XXXIV. Serratia Bizio 1823, 288a1. In: Bergey's manual of systematic bacteriology, 2nd edn., vol. 2, part B /D.J. Brenner, N.R. Krieg, J.T. Staley (eds.), Springer Science and Business Media, New York, NY, 2005: 799-811.
- Mühldorfer K., Speck S., Kurth A., Lesnik R., Freuling C., Müller T., Kramer-Schadt S., Wibbelt G. Diseases and causes of death in European bats: dynamics in disease susceptibility and infection rates. PLoS ONE, 2011, 6: e29773 (doi: 10.1371/journal.pone.0029773).
- Stock I., Grueger T., Wiedemann B. Natural antibiotic susceptibility of strains of Serratia mar-cescens and the S. liquefaciens complex: S. liquefaciens sensu stricto, S. proteamaculans and S. grimesii. International Journal of Antimicrobial Agents, 200Э, 22(1): Э5-47 (doi: 10.1016/s0924-8579(02)00163-2).
- Skerman V.B.D., McGowan V., Sneath, P.H.A. Approved lists of bacterial names. International Journal of Systematic and Evolutionary Microbiology, 1980, 30(1): 225-420 (doi: 10.1099/00207713-Э0-1-225).
- Bollet C., Grimont P., Gainnier M., Geissler A., Sainty J.M., De Micco P. Fatal pneumonia due to Serratia proteamaculans subsp. quinovora. Journal of Clinical Microbiology, 199Э, 31(2): 444445 (doi: 10.1128/jcm.31.2.444-445.1993).
- Mahlen S.D. Serratia infections: from military experiments to current practice. Clinical Microbiology Reviews, 2011, 24(4): 755-791 (doi: 10.1128/CMR.00017-11).
- Ajithkumar B., Ajithkumar V.P., Iriye R., Doi Y., Sakai T. Spore-forming Serratia marcescens subsp. sakuensis subsp. nov., isolated from a domestic wastewater treatment tank. International Journal of Systematic and Evolutionary Microbiology, 200Э, 53(1): 25Э-258 (doi: 10.1099/ijs.0.02158-0).
- Su C., Xiang Z., Liu Y., Zhao X., Sun Y., Li Z., Li L., Chang F., Chen T., Wen X., Zhou Y., Zhao F. ¿Analysis of the genomic sequences and metabolites of Serratia surfactantfaciens sp. nov. YD25T that simultaneously produces prodigiosin and serrawettin W2. BMC GGenomics, 2016, 17: 865 (doi: 10.1186/s12864-016-3171-7).
- Clements T., Ndlovu T., Khan W. Broad-spectrum antimicrobial activity of secondary metabolites produced by Serratia marcescens strains. Microbiological Research, 2019, 229: 126Э29 (doi: 10.1016/j.micres.2019.126329).
- Harris A.K.P., Williamson N.R., Slater H., Cox A., Abbasi S., Foulds I., Simonsen H.T., Leeper F.J., Salmond G.P.C. The Serratia gene cluster encoding biosynthesis of the red antibiotic, prodigiosin, shows species- and strain-dependent genome context variation. Microbiology, 2004, 150(11): 3547-3560 (doi: 10.1099/mic.0.27222-0).
- Hahn M. The rising threat of fungicide resistance in plant pathogenic fungi: Botrytis as a case study. Journal of Chemical Biology, 2014, 7(4): 133-141 (doi: 10.1007/s12154-014-0113-1).
- Rodel J., Mellmann A., Stein C., Alexi M., Kipp F., Edel B., Dawczynski K., Brandt C., Seidel L., Pfister W., Luffler B., Straube E. Use of MALDI-TOF mass spectrometry to detect nosocomial outbreaks of Serratia marcescens and Citrobacter freundii. European Journal of Clinical Microbiology & Infectious Diseases, 2019, 38: 581-591 (doi: 10.1007/s10096-018-03462-2).
- Moehario LH., Tjoa E., Putranata H., Joon S., Edbert D., Robertus T. Performance of TDR-300B and VITEK®2 for the identification of Pseudomonas aeruginosa in comparison with VI-TEK®-MS. Journal of International Medical Research, 2021, 49(2): 30006052198989 (doi: 10.1177/0300060521989893).
- Strejcek M., Smrhova T., Junkova P., UhlikFront O. Whole-cell MALDI-TOF MS versus 16S rRNA gene analysis for identification and dereplication of recurrent bacterial isolates. Frontiers in Microbiology, 2018, 9: 1294 (doi: 10.3389/fmicb.2018.01294).
- Crowley E., Bird P., Fisher K., Goetz K., Boyle M., Benzinger M.J., Jr, Juenger M., Agin J., Goins D., Johnson R., Collaborators. Evaluation of the VITEK 2 Gram-Negative (GN) Microbial Identification Test Card: collaborative study. Journal of AOAC International, 2012, 95(3): 778-785 (doi: 10.5740/jaoacint.CS2011_17).
- Vagelas I., Sugar I.R. Potential use of olive mill wastewater to control plant pathogens and post harvest diseases. Carpathian Journal of Food Science & Technology, 2020, 12(4): 140-145 (doi: 10.34302/crpjfst/2020.12.4.14).
- Vagelas I.K., Giurgiulescu L. Bioactivity of olive oil mill wastewater against grey mould disease. Carpathian Journal of Food Science & Technology, 2019, 11(4): 161-164 (doi: 10.34302/2019.11.4.15).
- Vagelas I.K. Efficacy of Pseudomonas oryzihabitans as a biocontrol agent of root pathogens. Thesis (PhD). University of Reading, UK, 2002.
- Vagelas I., Kalorizou H., Papachatzis A., Botu M. Bioactivity of olive oil mill wastewater against plant pathogens and post-harvest diseases. Biotechnology & Biotechnological Equipment, 2009, 23(2): 1217-1219 (doi: 10.1080/13102818.2009.10817641).
- Agarry O.O., Akinyosoye F.A., Adetuyi F.C. Antagonistic properties of microogranisms associated with cassava (Manihot esculenta, Crantz) products. African Journal of Microbiology, 2005, 4(7): 627-632 (doi: 10.5897/AJB2005.000-3114).
- Georgiakakis P., Papadatou E. Chiroptera. In: Deliverable 7, C-Phase of Study 7: "Monitoring and evaluation of conservation status mammal species of Community interest in Greece"/G. Papamichael, T. Arapis, K. Petkidi, I. Fytou, V. Chatirvasanis. Ministry of Environment, Energy and Climatic Change, Athens, Scholars Partnership and Consultancy Firms "ARAPIS THOMAS EY-AGGELOY, GEOANALYSI S.A. and PAPACHARISI ALEXANDRA THEODORA", Athens. 2015 (in Greek).
- Posteraro B., De Carolis E., Vella A., Sanguinetti M. MALDI-TOF mass spectrometry in the clinical mycology laboratory: identification of fungi and beyond. Expert Review of Proteomics, 2013, 10(2): 151-164 (doi: 10.1586/epr.13.8).
- Caroll K., Patel R. Systems for identification of bacteria and fungi. In: Manual of clinical microbiology, 11th edition /J.H. Jorgensen, K.C. Carroll, G. Funke, M.A. Pfaller, M.L. Landry, S.S. Richter, D.W. Warnock (eds.). ASM Press N.W., Washington, 2015: 29-43 (doi: 10.1128/9781555817381.ch4).
- Nomura F. Proteome-based bacterial identification using matrix-assisted laser desorption ioniza-tion-time of flight mass spectrometry (MALDI-TOF MS): A revolutionary shift in clinical diagnostic microbiology. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, 2015, 1854(6): 528-537 (doi: 10.1016/j.bbapap.2014.10.022).
- Ford B.A., Burham C.A. Optimization of routine identification of clinically relevant gramnegative bacteria by use of matrix-assisted laser desorption ionization-time of flight mass spectrometry and the Bruker Biotyper. Journal of Clinical Microbiology, 2013, 51(5): 1412-1420 (doi: 10.1128/JCM.01803-12).
- Hotta Y., Sato J., Sato H., Hosoda A., Tamura H. Classification of the genus Bacillus based on MALDI-TOF MS analysis of ribosomal proteins coded in S10 and spc operons. Journal of Agricultural and Food Chemistry, 2011, 59(10): 5222-5230 (doi: 10.1021/jf2004095).
- Seng P., Drancourt M., Couriet F., La Scola B., Fournier P-E., Rolain J.M., Raoult D. Ongoing revolution in bacteriology: routine identification of bacteria by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Clinical Infectious Diseases, 2009, 49(4): 543-551 (doi: 10.1086/600885).
- Cherkaoui A., Hibbs J., Emonet S., Tangomo M., Girard M., Francois P., Schrenzel J. Comparison of two matrix-assisted laser desorption ionization-time of flight mass spectrometry methods with conventional phenotypic identification for routine identification of bacteria to the species level. Journal of Clinical Microbiology, 2010, 48(4): 1169-1175 (doi: 10.1128/jcm.01881-09).
- Marko D.C., Saffeert R.T., Cunningham S.A., Hyman J., Walsh J., Arbefeville S., Howard W., Pruessner J., Safwat N., Cockerill F.R., Bossier A.D., Patel R., Richter S.S. Evaluation of the Bruker Biotyper and Vitek MS matrix-assisted laser desorption ionization-time of flight mass spectrometry systems for identification of nonfermenting gram-negative bacilli isolated from cultures from cystic fibrosis patients. Journal of Clinical Microbiology, 2012, 50(6): 2034-2039 (doi: 10.1128/jcm.00330-12).
- Mancini N., De Carolis E., Infurmari L., Vella A., Clementi N., Vaccaro L., Ruggeri A., Posteraro B., Burioni R., Clementi M., Sanguinetti M. Comparative evaluation of the Bruker Biotyper and Vitek MS matrix-assisted laser desorption ionization-time of flight (MALDI-TOF) mass spectrometry systems for identification of yeasts of medical importance. Journal of Clinical Microbiology, 2013, 51(7): 2453-2457 (doi: 10.1128/jcm.00841-13).
- Mather C.A., Rivera S.F., Butler-Wu S.M. Comparison of the Bruker Biotyper and Vitek MS matrix-assisted laser desorption ionization-time of flight mass spectrometry systems for identification of mycobacteria using simplified extraction protocols. Journal of Clinical Microbiology, 2014, 52(1): 130-138 (doi: 10.1128/JCM.01996-13).
- Alby K., Gilligan P., Miller M. Comparison of matrix-assisted laser desorption ionization-time of flight (MALDI-TOF) mass spectrometry platforms for the identification of gram-negative rods from patients with cystic fibrosis. Journal of Clinical Microbiology, 2013, 51(11): 3852-3854 (doi: 10.1128/JCM.01618-13).
- Kärpänoja P., Haruju I., Rantakokko-Jalava K., Haanperä M., Sarkkinen H. Evaluation of two matrix-assisted laser desorption ionization-time of flight mass spectrometry systems for identification of viridans group streptococci. European Journal of Clinical Microbiology & Infectious Diseases, 2014, 33: 779-788 (doi: 10.1007/s10096-013-2012-8).
- Sanguinetti M., Posteraro B. Mass spectrometry applications in microbiology beyond microbe identification: progress and potential. Expert Review of Proteomics, 2016, 13(10): 965-977 (doi: 10.1080/14789450.2016.1231578).
- Ramesh Babu N.G., Simrah Fathima K.A, Nandhini V., Nandhini V. Extraction of prodigiosin from Serratia marcescens and its application as an antibacterial spray. IP International Journal of Medical Microbiology and Tropical Diseases, 2019, 5(4): 207-209 (doi: 10.18231/j.ijmmtd.2019.047). Batah R., Loucif L., Olaitan A.O., Boutefnouchet N., Allag H., Rolain, J.M. Outbreak of Serratia marcescens coproducing ArmA and CTX-M-15 mediated high levels of resistance to aminoglycoside and extended-spectrum beta-lactamases, Algeria. Microbial Drug Resistance, 2015, 21(4): 470476 (doi: 10.1089/mdr.2014.0240).
- Claydon M.A., Davey S.N., Edwards-Jones V., Gordon D.B. The rapid identification of intact microorganisms using mass spectrometry. Nature Biotechnology, 1996, 14: 1584-1586 (doi: 10.1038/nbt1196-1584).
- Holland R.D., Wilkes J.G., Rafii F., Sutherland J.B., Persons C.C., Voorhees K.J., Lay J.O., Jr. Rapid identification of intact whole bacteria based on spectral patterns using matrix-assisted laser desorption/ionization with time-of-flight mass spectrometry. Rapid Communications in Mass Spectrometry, 1996, 10(10): 1227-1232 (doi: 10.1002/(SICI)1097-0231(19960731)10:10<1227::AID-RCM659-3.0.CO;2-6).
- Dieckmann R., Graeber I., Kaesler I., Szewzyk U., von Döhren H. Rapid screening and derep-lication of bacterial isolates from marine sponges of the Sula Ridge by Intact-Cell-MALDI-TOF mass spectrometry (ICM-MS). Applied Microbiology and Biotechnology, 2005, 67: 539-548 (doi: 10.1007/s00253-004-1812-2).
- Ghyselinck J., van Hoorde K., Hoste B., Heylen K., De Vos P. Evaluation of MALDI-TOF MS as a tool for high-throughput dereplication. Journal of Microbiological Methods, 2011, 86(3): 327336 (doi: 10.1016/j.mimet.2011.06.004).
- Spitaels F., Wieme A.D., Vandamme P. MALDI-TOF MS as a novel tool for dereplication and characterization of microbiota in bacterial diversity studies. In: Applications of mass spectrometry in microbiology: from strain characterization to rapid screening for antibiotic resistance /P. Demi-rev, T.R. Sandrin (eds.). Springer, Cham, 2016: 235-256 (10.1007/978-3-319-26070-9_9).
- Mellmann A., Cloud J., Maier T., Keckevoet U., Ramminger I., Iwen P., Dunn J., Hall G., Wilson D., LaSala P., Kostrzewa M., Harmsen D. Evaluation of matrix-assisted laser desorption ionization-time-of-flight mass spectrometry in comparison to 16S rRNA gene sequencing for species identification of nonfermenting bacteria. Journal of Clinical Microbiology, 2008, 46(6): 1946-1954 (doi: 10.1128/JCM.00157-08).
- Uhlik O., Strejcek M., Junkova P., Sanda M., Hroudova M., Vlcek C., Mackova M., Macek T. Matrix-assisted laser desorption ionization (MALDI)-time of flight mass spectrometry- and MALDI Biotyper-based identification of cultured biphenyl-metabolizing bacteria from contaminated horseradish rhizosphere soil. Applied and Environmental Microbiology, 2011, 77(19): 68586866 (doi: 10.1128/AEM.05465-11).
- Koubek J., Uhlik O., Jecna K., Junkova P., Vrkoslavova J., Lipov J., Kurzawova V., Macek T., Mackova M. Whole-cell MALDI-TOF: rapid screening method in environmental microbiology. International Biodeterioration & Biodegradation, 2012, 69: 82-86 (doi: 10.1016/j.ibiod.2011.12.007).
- Wieser A., Schneider L., Jung J., Schubert S. MALDI-TOF MS in microbiological diagnostics — identification of microorganisms and beyond (mini review). Applied Microbiology and Biotechnology, 2012, 93: 965-974 (doi: 10.1007/s00253-011-3783-4).
- Seng P., Abat C., Rolain J.M., Colson P., Lagier J.-C., Gouriet F., Fournier P.E., Drancourt M., La Scola B., Raoult D. Identification of rare pathogenic bacteria in a clinical microbiology laboratory: impact of MALDI-TOF mass spectrometry. Journal of Clinical Microbiology, 2013, 51(7): 2182-2194 (doi: 10.1128/JCM.00492-13).
- Fenselau C., Demirev P.A. Characterization of intact microorganisms by MALDI mass spectrometry. Mass Spectrometry Reviews, 2001, 20(4): 157-171 (doi: 10.1002/mas.10004).
- Lay J.O. Jr. MALDI-TOF mass spectrometry of bacteria. Mass Spectrometry Reviews, 2001, 20(4): 172-194 (doi: 10.1002/mas.10003).
- Newman M.M., Kloepper L.N., Duncan M., McInroy J.A., Kloepper J.W. Variation in bat guano bacterial community composition with depth. Frontiers in Microbiology, 2018, 9: 914 (doi: 10.3389/fmicb.2018.00914).
- Veikkolainen V., Vesterinen E.J., Lilley T.M., Pulliainen A.T. Bats as reservoir hosts of human bacterial pathogen, Bartonella mayotimonensis. Emerging Infectious Diseases, 2014, 20(6): 960-967 (doi: 10.3201/eid2006.130956).
- Wolkers-Rooijackers J., Rebmann K., Bosch T., Hazeleger W. Fecal bacterial communities in insectivorous bats from the Netherlands and their role as a possible vector for foodborne diseases. Acta Chiropterologica, 2019, 20: 475 (doi: 10.3161/15081109acc2018.20.2.017).
- Banskar S., Bhute S.S., Suryavanshi M.V., Punekar S., Shouche Y.S. Microbiome analysis reveals the abundance of bacterial pathogens in Rousettus leschenaultii guano. Scientific Reports, 2016, 6: 36948 (doi: 10.1038/srep36948).
- Selvin J., Lanong S., Syiem D., De Mandal S., Kayang H., Kumar N.S., Kiran G.S. Culture-dependent and metagenomic analysis of lesser horseshoe bats' gut microbiome revealing unique bacterial diversity and signatures of potential human pathogens. Microbial Pathogenesis, 2019, 137: 103675 (doi: 10.1016/j.micpath.2019.103675).
- AL-Ghanem M.M. Serratia A novel source of secondary metabolites. Advances in Biotechnology & Microbiology, 2018, 11(3): 555814 (doi: 10.19080/AIBM.2018.11.555814).
- Bhadra B., Ro P., Chakraborty R. Serratia ureilytica sp. nov., a novel urea-utilizing species. International Journal of Systematic and Evolutionary Microbiology, 2005, 55(5): 2155-2158 (doi: 10.1099/ijs.0.63674-0).
- Frankowski J., Lorito M., Scala F., Schmid R., Berg G., Bahl H. Purification and properties of two chitinolytic enzymes of Serratia plymuthica HRO-C48. Archives of Microbiology, 2001, 176(6): 421-426 (doi: 10.1007/s002030100347).
- Czajkowski R., Wolf J.M. Draft genome sequence of the biocontrol strain Serratia plymuthica A30, isolated from rotting potato tuber tissue. Journal of Bacteriology, 2012, 194: 6999-7000 (doi: 10.1128/jb.01699-12).
- Petersen L.M., Tisa L.S. Friend or foe? A review of the mechanisms that drive Serratia towards diverse lifestyles. Canadian Journal of Microbiology, 2013, 59(9): 627-640 (doi: 10.1139/cjm-2013-0343).
- Kimyon Ö., Das T., Ibugo A.I., Kutty S.K., Ho K.K., Tebben J., Kumar N., Manefield M. Serratia secondary metabolite prodigiosin inhibits Pseudomonas aeruginosa biofilm development by producing reactive oxygen species that damage biological molecules. Frontiers in Microbiology, 2016, 7: 972 (doi: 10.3389/fmicb.2016.00972).
- Stankovic N., Senerovic L., Ilic-Tomic T., Vasiljevic B., Nikodinovic-Runic J. Properties and applications of undecylprodigiosin and other bacterial prodigiosins. Applied Microbiology and Biotechnology, 2014, 98(9): 3841-3858 (doi. 10.1007/s00253-014-5590-1).