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Doktorska Disertacija Univerzitet u Novom Sadu Prirodno-matematički fakultet Departman za biologiju i ekologiju MSc Olivera Babić Karakterizacija zemljišnih cijanobakterijskih sojeva izolovanih iz šumskih ekosistema planinskih područja Republike Srbije -Doktorska disertacija- U Novom Sadu, 2018. PREDGOVOR Zahvaljujem se svima na Departmanu za biologiju i ekologiju i Prirodno-matematičkom fakultetu koji su omogućili izradu ove disertacije u okviru istraživanja na projektu „Biosenzing tehnologije i globalni sistem za kontinuirana istraživanja i integrisano upravljanje ekosistemima“ (Evidencioni broj projekta: III 43002) koji fininsira Ministartsvo prosvete, nauke i tehnološkog razvoja Republike Srbije i na projektu “Identification and characterization of cyanobacterial toxins based on their interaction with basic cellular detoxification systems in zebrafish (Danio rerio) and zooplankton Daphnia magna (IZ73ZO_152274/1)“ koje finansira Švajcarska. Posebnu zahvalnost dugujem svojoj mentorki, prof. dr Jelici Simeunović, za pomoć pri izradi i pisanju ove disertacije, spremnosti da svoje znanje podeli sa mnom kao i da omogući moje usavršavanje u Švajcarskoj. Takođe veliku zahvalnost dugujem predsedniku komisije prof. dr Zorici Svirčev na pomoći i korisnim savetima i doprinosu mog odlaska i usavršavanja u Finskoj. Hvala članovima komisije, prof. dr Draganu Radnoviću i prof. dr Simonidi Đurić na konstruktivnim i stručnim sugestijama. Hvala dr Ivici Tamaš na pomoći i savetima koji su mi pomogli pri pisanju disertacije. Veliku zahvalnost na pomoći u izradi eksperimentalnog dela disertacije dugujem dr Mileni Rašeti i Filipu Šibulu sa Departmana za hemiju kao i dr Tanji Tunić, dr Varji Knežević i Šandoru Šipošu sa Departmana za biologiju i ekologiju. Veliko hvala i dr Ivanu Milovanoviću (FINS) na pomoći prilikom izrade disertacije. Posebnu zahvalnost dugujem dr Petri Marić sa Instituta Ruđer Bošković iz Zagreba za svu pomoć pruženu tokom izrade ove doktorske disertacije. Iskrenu zahvalnost dugujem svim bivšim i sadašnjim članovima Katedre za mikrobiologiju, svim profesorima i kolegama doktorantima, na pomoći i podršći. Zahvaljujem se prijateljima na bezgraničnom razumevanju i nesebičnoj podršci. Najveću zahvalnost dugujem svojoj porodici pre svega svojim roditeljma, Jeleni i Branku, bez čije ljubavi, podrške i razumevanja ovaj rad ne bi bio moguć. SADRŽAJ 1. UVOD 1 1.1. Opšti deo 1 1.1.1. Morfološke karakteristike cijanobakterija 2 1.1.2. Klasifikacija 6 1.1.3. Fiziologija cijanobakterija 10 1.2. Biološki aktivna jedinjenja cijanobakterija 13 1.2.1. Masne kiseline 15 - Mehanizmi sinteze masnih kiselina 16 1.2.2. Antimikrobna jedinjenja 17 a) Alkaloidi 17 b) Peptidi 18 c) Terpenoidi 18 d) Masne kiseline 18 1.2.3. Antioksidativna jedinjenja 19 a) Fikocijanin 20 b) Karotenoidi 20 c) Fenoli 20 d) Enzimski antioksidansi 20 1.2.4. Toksini 21 1.2.4.1. Funkcionalne grupe cijanotoksina 23 1) Hepatotoksini 23 a) Mikrocistini 24 Biosinteza mikrocistina 25 Unos mikrocistina i mehanizam delovanja u eukariotskim ćelijama 26 b) Nodularin 26 c) Cilindrospermopsin 27 2) Neurotoksini 28 a) Anatoksini 28 b) Saksitoksin 29 Genotoksičnost cijanobakterija 30 1.2.4.2. Sudbina cijanotoksina u terestričnim ekosistemima 30 1.2.4.3. Metode detekcije cijanotoksina 31 1) Analitičke metode 31 2) Bioanalitičke metode 32 3) Molekularne metode 32 4) Biološki eseji 33 a) Artemia salina bioesej 33 b) Daphnia magna bioesej 34 c) Danio rerio bioesej 34 1.3. Rasprostranjenost cijanobakterija 36 1.4. Cijanobakterije terestričnih staništa i njihove adaptivne strategije 38 1.5. Uloga cijanobakterija u funkcionisanju zemljišnih ekosistema 40 1.5.1. Uloga cijanobakterija u kruženju biogenih elemenata 41 1.5.2. Produkcija egzopolisaharida 41 - Sastav i makromolekularne karakteristike egzopolisaharida 42 1.5.3. Naseljavanje „ogoljenih“ zemljišta 43 1.6. Upotreba terestričnih cijanobakterija 45 2. CILJEVI ISTRAŽIVANJA I HIPOTEZE 48 3. MATERIJAL I METODE RADA 50 3.1. Uzorkovanje zemljišta 50 3.2. Izolacija i determinacija izolovanih terestričnih cijanobakterija 53 3.3. Identifikacija cijanobakterijskih sojeva korišćenjem dela genske sekvence 16S 55 rRNK gena 3.3.1. Izolacija i purifikacija genomske DNK 55 3.4. Sekvencioniranje dela genske sekvence 16S rRNK gena 56 3.4.1. Prečišćavanje PCR proizvoda 57 3.4.2. Određivanje koncentracije DNK 57 3.4.3. Sekvenciranje dela genske sekvence 16S rRNK gena 57 3.5. Metod za utvrđivanje produkcije biomase cijanobakterijskih sojeva 58 3.6. Metod za utvrđivanje produkcije fikobilinskih pigmenata kod cijanobakterija 58 3.7. Ispitivanje miksotrofnog rasta - određivanje uticaja glukoze i saharoze na 59 produkciju biomase i fikobiliproteinskih pigmenata 3.8. Određivanje sadržaja ugljenih hidrata (PSA test) 59 3.9. Testiranje biološke aktivnosti cijanobakterija 61 3.9.1. Priprema ekstrakata cijanobakterija za detekciju biološki aktivnih 61 materija (BAM) 3.9.2. Određivanje antibakterijske aktivnosti cijanobakterija 61 3.9.2.1. Disk-difuziona metoda 62 3.9.2.2. Određivanje minimalne inhibitorne koncentracije (MIC) i minimalne 63 baktericidne koncentracije (MBC) cijanobakterijskih ekstrakata primenom mikrodilucione metode 3.9.3. Hemijska karakterizacija i određivanje sastava masnih kiselina nakon 64 transesterifikacije sa bor(III)-fluoridom metodom gasne hromatografije (GC-FID) 3.9.4. Određivanje antioksidativne aktivnosti cijanobakterija in vitro 66 3.9.4.1. Određivanje kapaciteta „hvatanja“ DPPH• radikala 66 3.9.4.2. Određivanje redoks kapaciteta FRAP metodom 67 3.9.5. Hemijska analiza fenolnog sastava cijanobakterija primenom LC/MS- 68 MS analize 3.9.6. Određivanje toksičnosti izolovanih cijanobakterija 68 3.9.6.1. Artemia salina bioesej 69 3.9.6.2. Daphnia magna bioesej 69 3.9.6.3. Danio rerio bioesej (DarT test) 71 3.10. qPCR metoda i ispitivanje efekta ekstrakta odabranog cijanobakterijskog soja na 72 ekspresiju 11 gena uključenih u signalne puteve kod model organizma Danio rerio 3.10.1. Ekstrakcija RNK 73 3.10.2. Sinteza cDNK 74 3.10.3. qPCR 74 3.11. Utvrđivanje toksigeničnosti cijanobakterija i detekcija prisutva mcy gena PCR 76 metodom 3.12. Statistička obrada podataka 77 4. REZULTATI I DISKUSIJA 78 4.1. Izolacija i determinacija izolovanih terestričnih cijanobakterija 78 4.2. Identifikacija cijanobakterijskih sojeva korišćenjem dela genske sekvence 16S 85 rRNK gena 4.3. Uticaj azota na produkciju biomase i sadržaj fikobiliproteinskih pigmenata 91 4.4. Ispitivanje miksotrofnog rasta – određivanje uticaja glukoze i saharoze na 97 produkciju biomase i sadržaj fikobiliproteinskih pigmenata 4.5. Određivanje sadržaja ugljenih hidrata – PSA test 111 4.6. Testiranje biološke aktivnosti terestričnih cijanobakterija izolovanih iz šumskih 115 ekosistema 4.7. Određivanje antimikrobne aktivnosti cijanobakterija 115 4.8. Hemijska karakterizacija i određivanje sastava masnih kiselina nakon 122 transesterifikacije sa bor(III)-fluoridom metodom gasne hromatografije (CG-FID) 4.9. Određivanje antioksidativne aktivnosti cijanobakterija in vitro 131 4.9.1. Rezultati određivanja kapaciteta „hvatanja“ DPPH• radikala 131 4.9.2. Rezultati određivanja redoks kapaciteta FRAP metodom 133 4.10. Hemijska analiza fenolnog sastava cijanobakterija primenom LC/MS-MS analize 136 4.11. Detekcija toksičnosti cijanobakterijskih sojeva izolovanih iz šumskih ekosistema 141 4.11.1. Artemia salina bioesej 142 4.11.2. Daphnia magna bioesej 145 4.11.3. Danio rerio bioesej 147 4.12. qPCR metoda i ispitivanje efekta ekstrakta odabranog cijanobakterijskog soja na ekspresiju 11 gena uključenih u signalne puteve kod model organizma Danio rerio 154 4.13. Utvrđivanje toksigeničnosti cijanobakterija i detekcija prisutva mcy gena PCR 160 metodom 5. ZAKLJUČAK 165 6. LITERATURA 168 7. PRILOZI 201 SKRAĆENICE AChE - acetilholinesteraza (acetylcholinesterase) AhR - aril-hidrokarbonski receptor (aryl hydrocarbon receptor) ahr2 gen- gen koji kodira aril hidrokarbonski receptor 2 (aryl hydrocarbon receptor 2) ALA - α-linoleinska kiselina APC – alofikocijanin (allophycocyanin) APX - askorbatna peroksidaza (ascorbate peroxidase) AR – androgeni receptor (androgene receptors) Ara - arabinoza ARA – arahidonska kiselina (arachidonic acid ) ASW – veštačka morska voda (artifical sea water) ATP - adenozin trifosfat (adenosine triphosphate) ATCC – Američka kolekcija kultura (American type culture collection) BAM – biološki aktivne materije bip gen– gen koji kodira vezujući imunoglobulinski protein (binding immunoglobulin protein) bp – bazni parovi (base pair) BLP – biološke lesne pokorice BMAA - β-metilamino-L-alanin BZP - biološke zemljišne pokorice cat gen– gen koji kodira katalazu (catalase) CAT – katalaza (catalase) CG-FID – gasna hromatografija sa plameno jonizacionim detektorom cry5 gen– gen koji kodira kriptohrom 5 (cryptochrome) CYN – cilindrospermopsin (cylindrospermopsin) cyp1a1 gen– gen koji kodira citohrom P450, familija 1, potfamilija 1 (cytochrome P450, family 1, subfamily A, polypeptide 1) DarT test – Danio rerio test (Danio rerio teratogenic assay) DHA - dokozaheksaenoinska kiselina D-MeAsp – D-eritro-β-metil asparaginska kiselina DMSO - dimetil sulfoksid (dimethyl sulfoxide) DPPH• radikal - 1,1-difenil-2-pikrilhidrazil radikal DRE - dioksin odgovorni elementi (dioxin responsive elements) ELISA – enzimski imuno-vezujući test (enzyme-linked immunosorbent assay) EPA - eikozapentaenoinska kiselina EPS- ekstracelularne polimerne supstance (extracellular polymeric substances) ER - estrogeni receptor (estrogen receptors) FET – testovi toksičnosti sa embrionima riba (fish embryo toxicity test) Gal - galaktoza GC – gasna
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