Abstract
Bark residual side streams from industries (Eucalyptus globulus—Eg and Picea abies—Pa) or from control of invasive species in Mediterranean countries (Acacia melanoxylon—Am and Acacia dealbata—Ad) are burned for energy production, although their high content of extractable compounds points to a possible valorization as sources of phytochemicals with antioxidant and antimicrobial activities. Non-polar and polar extracts were obtained, and their phenolic contents, antioxidant activity, antiquorum sensing and antimicrobial potential against several human pathogenic microbes (nine bacteria and two yeasts) were determined. Extraction yield ranged from 0.5 to 37% of barks dry weight varying with species and solvent used, and both water and ethanol extracts presented strong or very strong scavenging antioxidant ability. Eg and Pa non-polar extracts showed the lowest minimum inhibitory concentration for gram-positive bacteria (0.04–1.25 mg/mL), while Ad presented the best results among polar extracts regarding bacteria (0.16 mg/mL for K. pneumoniae) and yeast strains (0.02–0.04 mg/mL). Non-polar extracts showed great response against both Candida species (MIC = 0.04–0.63 mg/mL). Each extract had different antimicrobial activity showing that species and solvents can be used to tailor compounds to target specific pathogens. Information regarding these bioactive extracts from residual forest side streams can provide possible utilization routes for natural compounds recovery prior to combustion.
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Abbreviations
- EgH:
-
Eucalyptus globulus n-hexane extract
- PaH:
-
Picea abies n-hexane extract
- AmH:
-
Acacia melanoxylon n-hexane extract
- AdH:
-
Acacia dealbata n-hexane extract
- EgET:
-
Eucalyptus globulus ethanol extract
- PaET:
-
Picea abies ethanol extract
- AmET:
-
Acacia melanoxylon ethanol extract
- AdET:
-
Acacia dealbata ethanol extract
- EgW:
-
Eucalyptus globulus water extract
- PaW:
-
Picea abies water extract
- AmW:
-
Acacia melanoxylon water extract
- AdW:
-
Acacia dealbata water extract
References
Alfredsen G, Solheim H, Slimestad R (2008) Antifungal effect of bark extracts from some European tree species. Eur J For Res 127:387–393. https://doi.org/10.1007/s10342-008-0222-x
Angelis A, Hubert J, Aligiannis N, Michalea R, Abedini A, Nuzillard JM, Gangloff SC, Skaltsounis AL, Renault JH (2016) Bio-guided isolation of methanol-soluble metabolites of common spruce (Picea abies) bark by-products and investigation of their dermo-cosmetic properties. Molecules 21:1586. https://doi.org/10.3390/molecules21111586
Ávila F, Theoduloz C, López-Alarcón C, Dorta E, Schmeda-Hirschmann G (2017) Cytoprotective mechanisms mediated by polyphenols from Chilean native berries against free radical-induced damage on AGS cells. Oxid Med Cell Longev 2017:1–13. https://doi.org/10.1155/2017/9808520
Burčová Z, Kreps F, Greifová M, Jablonský M, Ház A, Schmidt Š, Šurina I (2018) Antibacterial and antifungal activity of phytosterols and methyl dehydroabietate of Norway spruce bark extracts. J Biotechnol 282:18–24. https://doi.org/10.1016/j.jbiotec.2018.06.340
Chang ST, Wu JH, Wang SY, Kang PL, Yang NS, Shyur LF (2001) Antioxidant activity of extracts from Acacia confusa bark and heartwood. J Agric Food Chem 49:3420–3424. https://doi.org/10.1021/jf0100907
Chemetova C, Fabião A, Gominho J, Ribeiro H (2018) Range analysis of Eucalyptus globulus bark low-temperature hydrothermal treatment to produce a new component for growing media industry. Waste Manag 79:1–7. https://doi.org/10.1016/j.wasman.2018.07.019
Co M, Fagerlund A, Engman L, Sunnerheim K, Sjöberg PJ, Turner C (2012) Extraction of antioxidants from spruce (Picea abies) bark using eco-friendly solvents. Phytochem Anal 23:1–11. https://doi.org/10.1002/pca.1316
Cowan MM (1999) Plant products as antimicrobial agents. Clin Microbiol Rev 12:564–582. https://doi.org/10.1128/CMR.12.4.564
Defoirdt T, Brackman G, Coenye T (2013) Quorum sensing inhibitors: how strong is the evidence? Trends Microbiol 21:619–624. https://doi.org/10.1016/j.tim.2013.09.006
Dezsi Ș, Bădărău AS, Bischin C, Vodnar DC, Silaghi-Dumitrescu R, Gheldiu AM, Mocan A, Vlase L (2015) Antimicrobial and antioxidant activities and phenolic profile of Eucalyptus globulus Labill. and Corymbia ficifolia (F. Muell.) K.D. Hill & L.A.S. Johnson Leaves. Molecules 20:4720–4734. https://doi.org/10.3390/molecules20034720
Eggler AL, Gay KA, Mesecar AD (2008) Molecular mechanisms of natural products in chemoprevention: induction of cytoprotective enzymes by Nrf2. Mol Nutr Food Res 52(Suppl 1):S84–S94. https://doi.org/10.1002/mnfr.200700249
Ferreira JPA, Miranda I, Gominho J, Pereira H (2015) Selective fractioning of Pseudotsuga menziesii bark and chemical characterization in view of an integrated valorization. Ind Crops Prod 74:998–1007. https://doi.org/10.1016/j.indcrop.2015.05.065
Forman HJ, Davies KJA, Ursini F (2014) How do nutritional antioxidants really work: nucleophilic tone and para-hormesis versus free radical scavenging in vivo. Free Radic Biol Med 66:24–35. https://doi.org/10.1016/j.freeradbiomed.2013.05.045
Hafizoglu H, Holmbom B (1995) Chemical composition of extractives from Abies nordmanniana. Holz Roh- Werkst 53:273–275. https://doi.org/10.1007/s001070050088
Hubert J, Angelis A, Aligiannis N, Rosalia M, Abedini A, Bakiri A, Reynaud R, Nuzillard JM, Gangloff SC, Skaltsounis AL, Renault JH (2016) In vitro dermo-cosmetic evaluation of bark extracts from common temperate trees. Planta Med 82:1351–1358. https://doi.org/10.1055/s-0042-110180
Ignat I, Radu DG, Volf I, Pag AI, Popa VI (2013) Antioxidant and antibacterial activities of some natural polyphenols. Cell Chem Technol 47:387–399. https://doi.org/10.13040/IJPSR.0975-8232.7(1).76-84
Jablonsky M, Nosalova J, Sladkova A, Haz A, Kreps F, Valka J, Miertus S, Frecer V, Ondrejovic M, Sima J, Surina I (2017) Valorisation of softwood bark through extraction of utilizable chemicals. A review. Biotechnol Adv 35:726–750. https://doi.org/10.1016/j.biotechadv.2017.07.007
Kalia VC (2013) Quorum sensing inhibitors: an overview. Biotechnol Adv 31:224–245. https://doi.org/10.1016/j.biotechadv.2012.10.004
Kemppainen K, Ranta L, Sipilä E, Östman A, Vehmaanperä J, Puranen T, Langfelder K, Hannula J, Kallioinen A, Siika-Aho M, Sipilä K, Von Weymarn N (2012) Ethanol and biogas production from waste fibre and fibre sludge—the FibreEtOH concept. Biomass Bioenerg 46:60–69. https://doi.org/10.1016/j.biombioe.2012.03.027
Kemppainen K, Siika-aho M, Pattathil S, Giovando S, Kruus K (2014) Spruce bark as an industrial source of condensed tannins and non-cellulosic sugars. Ind Crops Prod 52:158–168. https://doi.org/10.1016/j.indcrop.2013.10.009
Khan MSA, Zahin M, Hasan S, Husain FM, Ahmad I (2009a) Inhibition of quorum sensing regulated bacterial functions by plant essential oils with special reference to clove oil. Lett Appl Microbiol 49:354–360. https://doi.org/10.1111/j.1472-765X.2009.02666.x
Khan R, Islam B, Akram M, Shakil S, Ahmad A, Ali SM, Siddiqui M, Khan AU (2009b) Antimicrobial activity of five herbal extracts against multi drug resistant (MDR) strains of bacteria and fungus of clinical origin. Molecules 14:586–597. https://doi.org/10.3390/molecules14020586
Krogell J, Holmbom B, Pranovich A, Hemming J, Willför S (2012) Extraction and chemical characterization of Norway spruce inner and outer bark. Nord Pulp Pap Res J 27:006–017. https://doi.org/10.3183/NPPRJ-2012-27-01-p006-017
Kumar H, Kim I-S, More SV, Kim BW, Choi DK (2014) Natural product-derived pharmacological modulators of Nrf2/ARE pathway for chronic diseases. Nat Prod Rep 31:109–139. https://doi.org/10.1039/c3np70065h
Laboukhi-Khorsi S, Daoud K, Chemat S (2017) Efficient solvent selection approach for high solubility of active phytochemicals: application for the extraction of an antimalarial compound from medicinal plants. ACS Sustain Chem Eng 5:4332–4339. https://doi.org/10.1021/acssuschemeng.7b00384
Lima L, Miranda I, Knapic S, Quilhó T, Pereira H (2018) Chemical and anatomical characterization, and antioxidant properties of barks from 11 Eucalyptus species. Eur J Wood Prod 76:783–792. https://doi.org/10.1007/s00107-017-1247-y
Luís Â, Gil N, Amaral ME, Duarte AP (2012) Antioxidant activities of extracts from Acacia melanoxylon, Acacia dealbata and Olea europaea and alkaloids estimation. Int J Pharm Pharm Sci 4:225–231
Luís Â, Neiva D, Pereira H et al (2014) Stumps of Eucalyptus globulus as a source of antioxidant and antimicrobial polyphenols. Molecules 19:16428–16446. https://doi.org/10.3390/molecules191016428
Luís Â, Neiva DM, Pereira H, Gominho J, Domingues F, Duarte AP (2016) Bioassay-guided fractionation, GC–MS identification and in vitro evaluation of antioxidant and antimicrobial activities of bioactive compounds from Eucalyptus globulus stump wood methanolic extract. Ind Crops Prod 91:97–103. https://doi.org/10.1016/j.indcrop.2016.06.022
Miranda I, Gominho J, Mirra I, Pereira H (2012) Chemical characterization of barks from Picea abies and Pinus sylvestris after fractioning into different particle sizes. Ind Crops Prod 36:395–400. https://doi.org/10.1016/j.indcrop.2011.10.035
Miranda I, Gominho J, Mirra I, Pereira H (2013) Fractioning and chemical characterization of barks of Betula pendula and Eucalyptus globulus. Ind Crops Prod 41:299–305. https://doi.org/10.1016/j.indcrop.2012.04.024
Mocan A, Vodnar D, Vlase L, Crișan O, Gheldiu AM, Crișan G (2015) Phytochemical characterization of Veronica officinalis L., V. teucrium L. and V. orchidea Crantz from Romania and their antioxidant and antimicrobial properties. Int J Mol Sci 16:21109–21127. https://doi.org/10.3390/ijms160921109
Neiva DM, Gominh J, Fernandes L, Lourenço A, Chemetova C, Simões RMS, Pereira H (2016) The potential of hydrothermally pretreated industrial barks from E. globulus as a feedstock for pulp production. J Wood Chem Technol 36:383–392. https://doi.org/10.1080/02773813.2016.1184280
Neiva DM, Araújo S, Gominho J, Carneiro AC, Pereira H (2018a) Potential of Eucalyptus globulus industrial bark as a biorefinery feedstock: chemical and fuel characterization. Ind Crops Prod 123:262–270. https://doi.org/10.1016/j.indcrop.2018.06.070
Neiva DM, Araújo S, Gominho J, Carneiro AC, Pereira H (2018b) An integrated characterization of Picea abies industrial bark regarding chemical composition, thermal properties and polar extracts activity. PLoS ONE 13:e0208270. https://doi.org/10.1371/journal.pone.0208270
Nostro A, Germano MP, D’Angelo V, Marino A, Cannatelli MA (2000) Extraction methods and bioautography for evaluation of medicinal plant antimicrobial activity. Lett Appl Microbiol 30:379–384
Pinto PCR, Sousa G, Crispim F, Silvestre AJD, Neto CP (2013) Eucalyptus globulus bark as source of tannin extracts for application in leather industry. ACS Sustain Chem Eng 1:950–955. https://doi.org/10.1021/sc400037h
Pizzi A (2006) Recent developments in eco-efficient bio-based adhesives for wood bonding: opportunities and issues. J Adhes Sci Technol 20:829–846. https://doi.org/10.1163/156856106777638635
Prior RL, Wu X, Schaich K (2005) Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J Agric Food Chem 53:4290–4302. https://doi.org/10.1021/jf0502698
Rajan K, Nelson A, Adams JP, Carrier DJ (2017) Phytochemical recovery for valorization of loblolly pine and sweetgum bark residues. ACS Sustain Chem Eng 5:4258–4266. https://doi.org/10.1021/acssuschemeng.7b00243
Rodríguez-Rojo S, Visentin A, Maestri D, Cocero MJ (2012) Assisted extraction of rosemary antioxidants with green solvents. J Food Eng 109:98–103. https://doi.org/10.1016/j.jfoodeng.2011.09.029
Royer M, Prado M, García-Pérez ME, Diouf PN, Stevanovic T (2013) Study of nutraceutical, nutricosmetics and cosmeceutical potentials of polyphenolic bark extracts from Canadian forest species. Pharma Nutr 1:158–167. https://doi.org/10.1016/j.phanu.2013.05.001
Salem MZM, Elansary HO, Elkelish AA, Zeidler A, Ali HM, El-Hefny M, Yessoufou K (2016) In vitro bioactivity and antimicrobial activity of Picea abies and Larix decidua wood and bark extracts. BioResources 11:9421–9437
Santos SAO, Freire CSR, Domingues MRM, Silvestre AJ, Neto CP (2011) Characterization of phenolic components in polar extracts of Eucalyptus globulus labill. Bark by high-performance liquid chromatography-mass spectrometry. J Agric Food Chem 59:9386–9393. https://doi.org/10.1021/jf201801q
Savoia D (2012) Plant-derived antimicrobial compounds: alternatives to antibiotics. Future Microbiol 7:979–990. https://doi.org/10.2217/fmb.12.68
Scherer R, Godoy HT (2009) Antioxidant activity index (AAI) by the 2,2-diphenyl-1-picrylhydrazyl method. Food Chem 112:654–658. https://doi.org/10.1016/j.foodchem.2008.06.026
Seigler DS (2003) Phytochemistry of Acacia—sensu lato. Biochem Syst Ecol 31:845–873. https://doi.org/10.1016/S0305-1978(03)00082-6
Silva N, Fernandes Júnior A (2010) Biological properties of medicinal plants: a review of their antimicrobial activity. J Venom Anim Toxins Incl Trop Dis 16:402–413. https://doi.org/10.1590/S1678-91992010000300006
Souza-Alonso P, Rodríguez J, González L, Lorenzo P (2017) Here to stay. Recent advances and perspectives about Acacia invasion in Mediterranean areas. Ann For Sci 74:55. https://doi.org/10.1007/s13595-017-0651-0
Takeuchi TM, Pereira CG, Braga MEM, Maróstica MR, Leal PF, Meireles MAA (2009) Low pressure solvent extraction (solid-liquid-extraction, microwave assisted, and ultrasound assisted) from condimentary plants. In: Angela M, Meireles A (eds) Extracting bioactive compounds for food products: theory and applications. CRC Press, Boca Raton, pp 137–218
Tanase C, Cosarca S, Toma F, Mare A, Cosarca A, Man A, Miklos A, Imre S (2018a) Antibacterial activities of spruce bark (Picea abies L.) extract and its components against human pathogens. Rev Chim 69:1462–1467. https://doi.org/10.37358/RC.18.6.6347
Tanase C, Talmaciu AI, Bâra IC, Boz I, Volf I, Oroian S, Popa VI (2018b) New aspects of biomass waste valorization: spruce bark crude extracts as plant growth regulators. BioResources 13:3994–4007. https://doi.org/10.15376/biores.13.2.3994-4007
Tanigawa S, Fujii M, Hou DX (2007) Action of Nrf2 and Keap1 in ARE-mediated NQO1 expression by quercetin. Free Radic Biol Med 42:1690–1703. https://doi.org/10.1016/j.freeradbiomed.2007.02.017
Valimaa A, Honkalampihamalainen U, Pietarinen S, Willför S, Holmbom B, von Wright A (2007) Antimicrobial and cytotoxic knotwood extracts and related pure compounds and their effects on food-associated microorganisms. Int J Food Microbiol 115:235–243. https://doi.org/10.1016/j.ijfoodmicro.2006.10.031
Vasavi HS, Arun AB, Rekha PD (2013) Inhibition of quorum sensing in Chromobacterium violaceum by Syzygium cumini L. and Pimenta dioica L. Asian Pac J Trop Biomed 3:954–959. https://doi.org/10.1016/S2221-1691(13)60185-9
Wikaningtyas P, Sukandar EY (2016) The antibacterial activity of selected plants towards resistant bacteria isolated from clinical specimens. Asian Pac J Trop Biomed 6:16–19. https://doi.org/10.1016/j.apjtb.2015.08.003
Xiao J (2015) Dietary flavonoid aglycones and their glycosides: Which show better biological significance? Crit Rev Food Sci Nutr 57:1874–1905. https://doi.org/10.1080/10408398.2015.1032400
Zgurskaya HI, Rybenkov VV, Krishnamoorthy G, Leus IV (2018) Trans-envelope multidrug efflux pumps of Gram-negative bacteria and their synergism with the outer membrane barrier. Res Microbiol 169:351–356. https://doi.org/10.1016/j.resmic.2018.02.002
Zhao H, Dong J, Lu J, Chen J, Li Y, Shan L, Lin Y, Fan W, Gu G (2006) Effects of extraction solvent mixtures on antioxidant activity evaluation and their extraction capacity and selectivity for free phenolic compounds in Barley (Hordeum vulgare L.). J Agric Food Chem 54:7277–7286. https://doi.org/10.1021/jf061087w
Acknowledgments
We thank The Navigator Company for providing the Eucalyptus globulus bark and Mr. Asko Ojaniemi for providing the Picea abies bark used in this study.
Funding
The Forest Research Center (CEF) was financed by Fundação para a Ciência e a Tecnologia (FCT) under UID/AGR/00239/2013. CICS-UBI was supported by FEDER funds through the POCI-COMPETE 2020-Operational Program Competitiveness and Internationalization in Axis I-Strengthening research, technological development and innovation (Project POCI-01-0145-FEDER-007491) and National Funds by FCT-Foundation for Science and Technology (Project UID/Multi/00709/2013). The first author acknowledges a PhD scholarship (PD/BD/52697/2014) under the SUSFOR doctoral programme, and the second author the contract in the scientific area of microbiology that were both financed by FCT.
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Neiva, D.M., Luís, Â., Gominho, J. et al. Bark residues valorization potential regarding antioxidant and antimicrobial extracts. Wood Sci Technol 54, 559–585 (2020). https://doi.org/10.1007/s00226-020-01168-3
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DOI: https://doi.org/10.1007/s00226-020-01168-3