The influence of tannins purified from Eastern Mediterranean Region plants (Pinus brutia Ten. and Quercus coccifera L.) on carbon mineralization: Antimicrobial and antimutagenic evaluation

Year 2023, Volume: 7 Issue: 1, 60 - 69, 15.05.2023

Funda Ulusu , Cengiz Darıcı

https://doi.org/10.30616/ajb.1259084

Abstract

Tannins, which are polyphenols with a wide variety of quality-quantity that control the carbon and nitrogen cycle in forest ecosystems, are very interesting because of their protein binding abilities and forming a complex structure with other compounds. In this study, the purified tannin content of Pinus brutia Ten. and Quercus coccifera L., the two dominant plant species of the Eastern Mediterranean region, and the effect of these tannins on C dynamics in a forest soil (O and A horizon) were evaluated. In addition, antimicrobial effects of tannin extracts on Bacillus subtilis, Staphylococcus aureus and Proteus mirabilis bacteria by disc diffusion method and antimutagenic effects on Allium cepa root tip cells were evaluated. Total phenol (TP) and condense tannins (CT) concentrations of P. brutia and Q. coccifera leaves ranged from 0.78–1.33 μg/100mg DW and 4.68–1.35 μg/100mg DW, respectively. With the addition of tannin extract to the soils, C mineralization (27th day) was significantly reduced compared to the control group. Both P. brutia tannin extract (PTE) and Q. coccifera tannin extract (QTE) exhibited antibacterial activity in the range of 8±0.2–35±1.1 mm zone diameter by inhibiting their microbial growth against test microorganisms. In addition, tannin treatments caused a dose-dependent mitotic index decrease in onion root tip cells and a serious inhibition by showing toxic effects on mitotic division stages. As a result, our data showed that C mineralization in soil is affected by different tannin sources and these tannin extracts have significant antimicrobial activity against pathogens and cytotoxic activity in A. cepa root tip cells.

Keywords

Carbon mineralization, tannin, antimicrobial activity, antimutagenic activity

Supporting Institution

Çukurova Üniversitesi

Project Number

FEF2006YL59

Thanks

Supported by Cukurova University Research Projects Unit under Project no FEF2006YL59.

Doğu Akdeniz Bölgesi bitkilerinden (Pinus brutia Ten. ve Quercus coccifera L.) saflaştırılan tanenlerin karbon mineralizasyonu üzerindeki etkisi: Antimikrobiyal ve antimutajenik değerlendirme

Abstract

Orman ekosistemlerinde karbon ve nitrojen döngüsünü kontrol eden çok çeşitli kalite-niceliğe sahip polifenoller olan tanenler, protein bağlama yetenekleri ve diğer bileşiklerle kompleks bir yapı oluşturmaları nedeniyle oldukça ilgi çekicidir. Bu çalışmada, Doğu Akdeniz bölgesinin iki baskın bitki türü olan Pinus brutia Ten. ve Quercus coccifera L.'nın saflaştırılmış tanen içerikleri ve bu tanenlerin bir orman toprağında (O ve A horizonu) C dinamiklerine etkisi değerlendirilmiştir. Ayrıca tanen ekstraktlarının disk difüzyon yöntemi ile Bacillus subtilis, Staphylococcus aureus ve Proteus mirabilis bakterileri üzerindeki antimikrobiyal etkileri ve Allium cepa kök ucu hücreleri üzerindeki antimutajenik etkileri değerlendirilmiştir. P. brutia ve Q. coccifera yapraklarının toplam fenol (TP) ve kondanse tanen (CT) konsantrasyonları sırasıyla 0.78–1.33 μg/100mg DW ve 4.68–1.35 μg/100mg DW arasında değişmiştir. Topraklara tanen ekstraktı ilavesi ile C mineralizasyonu (27. gün) kontrol grubuna göre önemli ölçüde azalmıştır. Hem P. brutia tanen ekstresi (PTE) hem de Q. coccifera tanen ekstresi (QTE), test edilen mikroorganizmalara karşı 8±0.2–35±1.1 mm zon çapı aralığında antibakteriyel aktivite sergilemiştir. Ayrıca tanen uygulamaları soğan kök ucu hücrelerinde doza bağımlı mitotik indeks azalmasına ve mitotik bölünme evrelerinde toksik etki göstererek ciddi bir inhibisyona neden olmuştur. Sonuç olarak, elde edilen veriler topraktaki C mineralizasyonunun farklı tanen kaynaklarından etkilendiğini ve bu tanen ekstraktlarının patojenlere karşı önemli antimikrobiyal aktiviteye ve A. cepa kök ucu hücrelerinde sitotoksik aktiviteye sahip olduğunu göstermiştir.

Keywords

Karbon mineralizasyonu, tanen, antimikrobial aktivite, antimutajenik aktivite

Project Number

FEF2006YL59

References

• Abilleira F, Varela P, Cancela Á, Álvarez X, Sánchez Á, Valero E, et al. (2021). Tannins extraction from Pinus pinaster and Acacia dealbata bark with applications in the industry. Industrial Crops and Products 164: 113394.
• Adamczyk S, Kiikkilä O, Kitunen V, Smolander A, et al. (2013). Potential response of soil processes to diterpenes, triterpenes and tannins: Nitrification, growth of microorganisms and precipitation of proteins. Applied Soil Ecology 67: 47-52.
• Alizade Naini M, Mehrvarzi S, Zargari-Samadnejadi A, Tanideh N, Ghorbani M, Dehghanian A, Iraji A, et al. (2021). The antioxidant and anti-inflammatory effects of Quercus brantii extract on TNBS-induced ulcerative colitis in rats. Evidence-based Complementary and Alternative Medicine.
• AlSheikh HMA, Sultan I, Kumar V, Rather I. A, Al-Sheikh H, Tasleem Jan A, et al. (2020). Plant-based phytochemicals as possible alternative to antibiotics in combating bacterial drug resistance. Antibiotics 9(8): 480.
• Antunes-Ricardo M, Gutierrez-Uribe JO, Serna-Saldivar S (2015). Anti-inflammatory glycosylated flavonoids as therapeutic agents for treatment of diabetes-impaired wounds. Current Topics in Medicinal Chemistry 15(23): 2456-2463.
• Bardgett R (2016). Earth Matters: How soil underlies civilization. Oxford University Press.
• Barman A, Ray S (2022). Mitotic Index Reduction and Cytotoxic Effects of Leaf Aqueous Extract of Maesa macrophylla (Wall.) A. DC. in Allium cepa Root Tip Cells. Cytologia 87(2): 81-85.
• Barrajón-Catalán E, Fernández-Arroyo S, Saura D, Guillén E, Fernández-Gutiérrez A, Segura-Carretero A, Micol V, et al. (2010). Cistaceae aqueous extracts containing ellagitannins show antioxidant and antimicrobial capacity, and cytotoxic activity against human cancer cells. Food and Chemical Toxicology 48(8-9): 2273-2282.
• Bate-Smith EC (1975). Phytochemistry of proanthocyanidins. Phytochemistry 14(4): 1107-1113.
• Bauer AW, Kirby WM, Sherris JC, Turck M (1966). Antibiotic susceptibility testing by a standardized single disk method. American Journal of Clinical Pathology 45: 493-496.
• Bernal MP, Navarro A. F, Sanchez-Monedero MA, Roig A, Cegarra J, et al. (1998). Influence of sewage sludge compost stability and maturity on carbon and nitrogen mineralization in soil. Soil Biology and Biochemistry 30(3): 305-313.
• Bouyoucos G J (1951). A recalibration of the hydrometer method for making mechanical analysis of soils 1. Agronomy Journal 43(9): 434-438.
• Bridgham SD, Updegraff K, Pastor J (1998). Carbon, nitrogen, and phosphorus mineralization in northern wetlands. Ecology 79(5): 1545-1561.
• Bulut G, Haznedaroğlu MZ, Doğan A, Koyu H, Tuzlacı E (2017). An ethnobotanical study of medicinal plants in Acipayam (Denizli-Turkey). Journal of Herbal Medicine 10: 64-81.
• Cai A, Feng W, Zhang W, Xu M (2016). Climate, soil texture, and soil types affect the contributions of fine-fraction-stabilized carbon to total soil organic carbon in different land uses across China. Journal of Environmental Management 172: 2-9.
• Chandra H, Bishnoi P, Yadav A, Patni B, Mishra AP, et al. (2017). Antimicrobial resistance and the alternative resources with special emphasis on plant-based antimicrobials—a review. Plants 6(2): 16.
• Chupin L, Motillon C, Charrier-El Bouhtoury F, Pizzi A, Charrier B (2013). Characterisation of maritime pine (Pinus pinaster) bark tannins extracted under different conditions by spectroscopic methods, FTIR and HPLC. Industrial Crops and Products 49: 897-903.
• Ekambaram SP, Perumal SS, Balakrishnan A (2016). Scope of hydrolysable tannins as possible antimicrobial agent. Phytotherapy Research 30(7): 1035-1045.
• Elkady W M, Gonaid MH, Yousif MF, El-Sayed M, Omar HA (2021). Impact of Altitudinal Variation on the Phytochemical Profile, Anthelmintic and Antimicrobial Activity of Two Pinus Species. Molecules 26(11): 3170.
• Elrys AS, Desoky ESM, El-Maati MFA, Elnahal AS, Abdo AI, Raza S, Zhou J (2019). Can secondary metabolites extracted from Moringa seeds suppress ammonia oxidizers to increase nitrogen use efficiency and reduce nitrate contamination in potato tubers?. Ecotoxicology and Environmental Safety 185: 109689.
• Feng S, Zeng W, Luo F, Zhao J, Yang Z, Sun Q (2010). Antibacterial activity of organic acids in aqueous extracts from pine needles (Pinus massoniana Lamb.). Food Science and Biotechnology 19(1): 35-41.
• Ghazghazi H, Riahi L, Yangui I, Messaoud C, Rzigui T, Nasr Z (2022). Effect of Drought Stress on Physio-biochemical Traits and Secondary Metabolites Production in the Woody Species Pinus halepensis Mill. At a Juvenile Development Stage. Journal of Sustainable Forestry 1-17.
• Gomes de Melo J, de Sousa Araújo TA, e Castro TNDA, Lyra de Vasconcelos Cabral D, Do Desterro Rodrigues M, Carneiro do Nascimento S, et al. (2010). Antiproliferative activity, antioxidant capacity and tannin content in plants of semi-arid northeastern Brazil. Molecules 15(12): 8534-8542.
• Gonzalez-Hernandez MP, Karchesy J, Starkey EE (2003). Research observation: hydrolyzable and condensed tannins in plants of northwest Spain forests. Rangeland Ecology & Management/Journal of Range Management Archives 56(5): 461-465.
• Halvorson JJ, Gonzalez JM (2008). Tannic acid reduces recovery of water-soluble carbon and nitrogen from soil and affects the composition of Bradford-reactive soil protein. Soil Biology and Biochemistry 40(1): 186-197.
• Hassan A, Amjid I (2009). Gas chromatography-mass spectrometric studies of essential oil of Pinus roxburghaii stems and their antibacterial and antifungal activities. J Med Plant Res 3: 670-3.
• Hernes PJ, Hedges JI (2000). Determination of condensed tannin monomers in environmental samples by capillary gas chromatography of acid depolymerization extracts. Analytical Chemistry 72(20): 5115-5124.
• Ingold M, Wachendorf C, Buerkert A (2021). Net‐mineralization of organic matter and greenhouse gas emissions from Quebracho tannin‐enriched manure applied to acidic and alkaline soils. Journal of Plant Nutrition and Soil Science 184(5): 530-542.
• Ito H, Yamaguchi K, Kim TH, Khennouf S, Gharzouli K, Yoshida T (2002). Dimeric and Trimeric Hydrolyzable Tannins from Quercus coccifera and Quercus suber. Journal of Natural Products 65(3): 339-345.
• Jaramillo AF, Martinez JC, Flores P, Medina C, Rojas D, Díaz-Gómez A, et al. (2022). Condensed tannin resins extracted from Pinus radiata bark as a support matrix in carbon nanofiber-reinforced polymers. Polymer Bulletin 79(2): 743-762.
• Jones WP, Kinghorn AD (2012). Extraction of plant secondary metabolites. Natural Products Isolation 341-366.
• Kanchan B, Prerna B, Simran K (2020). Medicinal value of secondary metabolites of pines grown in Himalayan region of India. Research Journal of Biotechnology 15: 7.
• Kaushik D, Kaushik P, Kumar A, Rana AC, Sharma C, Aneja KR (2013). GC-MS analysis and antimicrobial activity of essential oil of Pinus roxburghii Sarg. from Northern India. Journal of Essential Oil Bearing Plants 16(4): 563-567.
• Kim H, Lee B, Yun KW (2013). Comparison of chemical composition and antimicrobial activity of essential oils from three Pinus species. Industrial Crops and Products 44: 323-329.
• Kraus TEC, Dahlgren RA, Zasoski RJ (2003). Tannins in nutrient dynamics of forest ecosystems-a review. Plant and Soil 256(1): 41-66.
• Kraus TEC, Zasoski RJ, Dahlgren RA (2004a). Fertility and pH effects on polyphenol and condensed tannin concentrations in foliage and roots. Plant and Soil 262: 95-109.
• Kraus TEC, Zasoski RJ, Dahlgren RA, Horwath WR, Preston CM (2004b). Carbon and nitrogen dynamics in a forest soil amended with purified tannins from different plant species. Soil Biology and Biochemistry 36(2): 309-321.
• Ku CS, Jang JP, Mun SP (2007). Exploitation of polyphenol-rich pine barks for potent antioxidant activity. Journal of Wood Science 53: 524-528.
• Kuiters AT (1990). Role of phenolic substances from decomposing forest litter in plant-soil interactions. Acta Botanica Neerlandica 39(4): 329-348.
• Kundu LM, Ray S (2017). Mitotic abnormalities and micronuclei inducing potentials of colchicine and leaf aqueous extracts of Clerodendrum viscosum Vent. in Allium cepa root apical meristem cells. Caryologia 70(1): 7-14.
• Kuo PC, Li YC, Kusuma AM, Tzen JT, Hwang TL, Ye GH, et al. (2021). Anti-inflammatory principles from the needles of Pinus taiwanensis hayata and in silico studies of their potential anti-aging effects. Antioxidants 10(4): 598.
• Lal R (2002). Soil carbon dynamics in cropland and rangeland. Environmental Pollution 116(3): 353-362.
• Landesman WJ, Dighton J (2010). Response of soil microbial communities and the production of plant-available nitrogen to a two-year rainfall manipulation in the New Jersey Pinelands. Soil Biology and Biochemistry 42(10): 1751-1758.
• Liu Y, Jiang M, Lu X, Lou Y, Liu B (2017). Carbon, nitrogen and phosphorus contents of wetland soils in relation to environment factors in Northeast China. Wetlands 37(1): 153-161.
• Lovieno P, Alfani A, Baath E (2010). Soil microbial community structure and biomass as affected by Pinus pinea plantation in two Mediterranean areas. Applied Soil Ecology 45(1): 56-63.
• Madritch MD, Jordan LM, Lindroth RL (2007). Interactive effects of condensed tannin and cellulose additions on soil respiration. Canadian Journal of Forest Research 37(10): 2063-2067.
• Makhlouf FZ, Squeo G, Barkat M, Trani A, Caponio F (2018). Antioxidant activity, tocopherols and polyphenols of acornoil obtained from Quercus species grown in Algeria. Food Research International 114: 208-213.
• Makkar HPS (2003). Quantification of tannins in tree and shrub foliage: a laboratory manual. Springer Science & Business Media.
• Makkar HPS, Singh B (1991). Effect of drying conditions on tannin, fibre and lignin levels in mature oak (Quercus incana) leaves. Journal of the Science of Food and Agriculture 54(3): 323-328.
• Mitić ZS, Jovanović B, Jovanović SČ, Stojanović-Radić ZZ, Mihajilov-Krstev T, Jovanović NM, et al. (2019). Essential oils of Pinus halepensis and P. heldreichii: Chemical composition, antimicrobial and insect larvicidal activity. Industrial Crops and Products 140: 111702.
• Norris CE, Preston CM, Hogg KE, Titus BD (2011). The influence of condensed tannin structure on rate of microbial mineralization and reactivity to chemical assays. Journal of Chemical Ecology 37(3): 311-319.
• Northup RR, Dahlgren RA, Yu Z (1995). Intraspecific variation of conifer phenolic concentration on a marine terrace soil acidity gradient; a new interpretation. Plant and Soil 171: 255-262.
• Nouri L, Nafchi AM, Karim AA (2014). Phytochemical, antioxidant, antibacterial, and α-amylase inhibitory properties of different extracts from betel leaves. Industrial Crops and Products 62: 47-52.
• Peng K, Jin L, Niu YD, Huang Q, McAllister TA, Yang HE, et al. (2018). Condensed tannins affect bacterial and fungal microbiomes and mycotoxin production during ensiling and upon aerobic exposure. Applied and Environmental Microbiology 84(5): 02274-17.
• Petins MMC, Sarria-Villa RA, Benítez RB, Corredor JAG (2021). Chemical modified tannins from Pinus patula bark for selective biosorption of gold in aqueous media. Journal of Environmental Chemical Engineering 9(5): 106162.
• Pizzi A (2003). Natural phenolic adhesives I: Tannin. Handbook of Adhesive Technology 2: 573-587.
• Qualls RG, Bridgham SD (2005). Mineralization rate of 14C-labelled dissolved organic matter from leaf litter in soils of a weathering chronosequence. Soil Biology and Biochemistry 37(5): 905-916.
• Ray S, Kundu LM, Goswami S, Roy GC, Chatterjee S, Dutta S, Chaudhuri A, Chakrabarti CS (2013). Metaphase arrest and delay in cell cycle kinetics of root apical meristems and mouse bone marrow cells treated with leaf aqueous extracts of Clerodendrum viscosum Vent. Cell Prolif. 46:109–117.
• Rencüzoğulları E, Kayraldız A, İla HB, Çakmak T, Topaktaş M (2001). The cytogenetic effects of sodium metabisulfite, a food preservative in root tip cells of Allium cepa L. Turkish Journal of Biology 25(4): 361-370.
• Rimmer DL (2006). Free radicals, antioxidants, and soil organic matter recalcitrance. European Journal of Soil Science 57(2): 91-94.
• Sakar MK, Şöhretoğlu D, Özalp M, Ekizoğlu M, Piacente S, Pizza C (2005). Polyphenolic compounds and antimicrobial activity of Quercus aucheri leaves. Turkish Journal of Chemistry 29(5): 555-559.
• Sancho-Knapik D, Sanz MÁ, Peguero-Pina JJ, Niinemets Ü, Gil-Pelegrín E (2017). Changes of secondary metabolites in Pinus sylvestris L. needles under increasing soil water deficit. Annals of Forest Science 74(1): 1-10.
• Satirapathkul C, Leela T (2011). Growth inhibition of pathogenic bacteria by extract of Quercus infectoria galls. Int J Biosci Biochem Bioinform 1: 26-31.
• Semwal P, Painuli S, Badoni H, Bacheti RK (2018). Screening of phytoconstituents and antibacterial activity of leaves and bark of Quercus leucotrichophora A. Camus from Uttarakhand Himalaya. Clinical Phytoscience 4(1): 1-6.
• Shah F, Nicolás C, Bentzer J, Ellström M, Smits M, Rineau F, et al. (2016). Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors. New Phytologist 209(4): 1705-1719.
• Siemens DH, Garner SH, Mitchell-Olds T, Callaway RM (2002). Cost of defense in the context of plant competition: Brassica rapa may grow and defend. Ecology 83(2): 505-517.
• Soto-García M, Rosales-Castro M, Escalona-Cardoso G N, Paniagua-Castro N (2016). Evaluation of hypoglycemic and genotoxic effect of polyphenolic bark extract from Quercus sideroxyla. Evidence-Based Complementary and Alternative Medicine 2016: 4032618.
• Treseder KK, Lennon JT (2015). Fungal traits that drive ecosystem dynamics on land. Microbiology and Molecular Biology Reviews 79(2): 243-262.
• Updegraff K, Pastor J, Bridgham SD, Johnston CA (1995). Environmental and substrate controls over carbon and nitrogen mineralization in northern wetlands. Ecological Applications 5(1): 151-163.
• Wafa N, Sofiane G, Mouhamed K (2016). The antioxidant and antimicrobial activities of flavonoids and tannins extracted from Phlomis bovei De Noé. European Journal of Experimental Biology 6(3): 55-61.
• Waldrop MP, Firestone MK (2004). Microbial community utilization of recalcitrant and simple carbon compounds: impact of oak-woodland plant communities. Oecologia 138(2): 275-284.
• Walkley A, Black IA (1934). An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science 37(1): 29-38.
• Wan X, Huang Z, He Z, Yu Z, Wang M, Davis MR, Yang Y (2015). Soil C: N ratio is the major determinant of soil microbial community structure in subtropical coniferous and broadleaf forest plantations. Plant and Soil 387: 103-116.
• Wang CC, Chen LG, Yang LL (2000). Cuphiin D1, the macrocyclic hydrolyzable tannin induced apoptosis in HL-60 cell line. Cancer Letters 149(1-2): 77-83.
• Weiss M, Simon M (1999). Consumption of labile dissolved organic matter by limnetic bacterioplankton: the relative significance of amino acids and carbohydrates. Aquatic Microbial Ecology 17(1): 1-12.
• Wu G, Gao J, Li H, Ren F, Liang D, Li X (2023). Shifts in plant and soil C, N, and P concentrations and C: N: P stoichiometry associated with environmental factors in alpine marshy wetlands in West China. Catena 221: 106801.
• Yang J, Choi WS, Kim KJ, Eom CD, Park MJ (2021). Investigation of active anti-inflammatory constituents of essential oil from Pinus koraiensis (Sieb. et Zucc.) wood in LPS-stimulated RBL-2H3 cells. Biomolecules 11(6): 817.
• Zhang H, Zou P, Zhao H, Qiu J, Mac Regenstein J, Yang X (2021). Isolation, purification, structure and antioxidant activity of polysaccharide from pinecones of Pinus koraiensis. Carbohydrate Polymers 251: 117078.
• Zhang QF, Laanbroek HJ (2018). The effects of condensed tannins derived from senescing Rhizophora mangle leaves on carbon, nitrogen and phosphorus mineralization in a Distichlis spicata salt marsh soil. Plant and Soil 433(1): 37-53.
• Zhang Y, Marschner P (2017). Soil amendment with high and low C/N residue-influence of low soil water content between first and second residue addition on soil respiration, microbial biomass and nutrient availability. Journal of Soil Science and Plant Nutrition 17(3): 594-608.
• Zhou D, Liu ZH, Wang DM, Li DW, Yang LN, Wang W (2019). Chemical composition, antibacterial activity and related mechanism of valonia and shell from Quercus variabilis Blume (Fagaceae) against Salmonella paratyphi a and Staphylococcus aureus. BMC Complementary and Alternative Medicine 19(1): 1-12.
• Zibilske LM, Bradford JM (2007). Oxygen effects on carbon, polyphenols, and nitrogen mineralization potential in soil. Soil Science Society of America Journal 71(1): 133-139.
• Zulfqar F, Akhtar MF, Saleem A, Akhtar B, Sharif A. Saleem U (2020). Chemical characterization, antioxidant evaluation, and antidiabetic potential of Pinus gerardiana (Pine nuts) extracts. Journal of Food Biochemistry 44(6): e13199.