Research Articles

Antibacterial and anticandidal activity of Tylosema esculentum (marama) extracts

Walter Chingwaru, Gyebi Duodu, Yolandi van Zyl, C.J. Schoeman, Runner T. Majinda, Sam O. Yeboah, Jose Jackson, Petrina T. Kapewangolo, Martha Kandawa-Schulz, Amanda Minnaar, Avrelija Cencic
South African Journal of Science | Vol 107, No 3/4 | a366 | DOI: https://doi.org/10.4102/sajs.v107i3/4.366 | © 2011 Walter Chingwaru, Gyebi Duodu, Yolandi van Zyl, C.J. Schoeman, Runner T. Majinda, Sam O. Yeboah, Jose Jackson, Petrina T. Kapewangolo, Martha Kandawa-Schulz, Amanda Minnaar, Avrelija Cencic | This work is licensed under CC Attribution 4.0
Submitted: 20 July 2010 | Published: 03 March 2011

About the author(s)

Walter Chingwaru, University of Maribor, Slovenia
Gyebi Duodu, University of Pretoria, South Africa
Yolandi van Zyl, University of Pretoria, South Africa
C.J. Schoeman, University of Pretoria, South Africa
Runner T. Majinda, University of Botswana, Botswana
Sam O. Yeboah, University of Botswana, Botswana
Jose Jackson, University of Botswana, Botswana
Petrina T. Kapewangolo, University of Namibia, Namibia
Martha Kandawa-Schulz, University of Namibia, Namibia
Amanda Minnaar, University of Pretoria, South Africa
Avrelija Cencic, University of Maribor, Slovenia

Abstract

Bean and tuber extracts of Tylosema esculentum (marama) – an African creeping plant – were obtained using ethanol, methanol and water. Based on information that T. esculentum is used traditionally for the treatment of various diseases, the antibacterial and anticandidal effects of tuber and bean extracts were investigated. The antimicrobial activity of the extracts was tested on methicillin-resistant Staphylococcus aureus (MRSA, ATCC 6538), Mycobacterium terrae (ATCC 15755), Corynebacterium diphtheriae (clinical) and Candida albicans (ATCC 2091). We performed the broth microdilution test for the determination of the minimum inhibitory concentration (MIC) and a method to determine survival of microorganisms after in vitro co-incubation with the highest concentrations of T. esculentum extracts, followed by assessment of colony counts. Ethanol and methanol (phenolic) bean extracts exhibited higher potency against bacteria and yeast than aqueous extracts. Marama bean seed coat crude ethanolic extract (MSCE) and seed coat polyphenolic fractions, especially soluble-bound fraction (MSCIB), were highly antimicrobial against M. terrae, C. diphtheriae and C. albicans. All marama bean polyphenolic fractions, namely cotyledon acidified methanol fraction (MCAM), seed coat acidified methanol fraction (MSCAM), cotyledon insoluble-bound fraction (MCIB), seed coat insoluble-bound fraction (MSCIB), cotyledon-free polyphenolic fraction (MCFP) and seed coat free polyphenolic fraction (MSCFP) had high antimicrobial effects as shown by low respective MIC values between 0.1 mg/mL and 1 mg/mL. These MIC values were comparable to those of control antimicrobials used: amphotericin B (0.5 mg/mL) and cesfulodin (0.1 mg/mL) against C. diphtheriae, streptomycin (1.0 mg/mL) and gentamicin (0.4 mg/mL) against M. terrae, and amphotericin B (0.05 mg/mL) against C. albicans. Marama seed coat soluble-esterified fraction (MSCS) had closer activity to that of cefsulodin against M. terrae. High amounts of phenolic substances, such as gallic acid, especially in the seed coats, as well as high amounts of phytosterols, lignans, certain fatty acids and peptides (specifically protease inhibitors) in the cotyledons contributed to the observed antibacterial and anticandidal activities. Marama extracts, especially phenolic and crude seed coat extracts, had high multi-species antibacterial and anticandidal activities at concentrations comparable to that of some conventional drugs; these extracts have potential use as microbicides.

Keywords

antibacterial; anticandidal; Candida albicans; Corynebacterium diphtheriae; methicillin-resistant Staphylococcus aureus; Mycobacterium terrae; plant extract

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References


Van der Maesen LJG. Tylosema esculentum (Burch.) A.Schreib. In: Brink M, Belay G, editors. PROTA 1: Cereals and pulses/Cereales et legumes secs. [book on CD-ROM]. Wageningen: PROTA; 2006.

McMurdo ME, Argo I, Phillips G, et al. Cranberry or trimethoprim for the prevention of recurrent urinary tract infections? A randomized controlled trial in older women. J Antimicrob Chemother. 2009;63(2):389–395. doi:10.1093/jac/dkn489, PMid:19042940, PMCid:2639265

Chan KH, Pan RN, Hsu MC, Hsu KF. Urinary elimination of ephedrines following administration of the traditional Chinese medicine preparation Kakkon-to. J Anal Toxicol. 2008;32(9):763–767. PMid:19021932

Chomnawang MT, Trinapakul C, Gritsanapan W. In vitro antigonococcal activity of Coscinium fenestratum stem extract. J Ethnopharmacol. 2009;122(3):445–449. doi:10.1016/j.jep.2009.01.036, PMid:19429310

Tomczykowa M, Tomczyk M, Jakoniuk P, Tryniszewska E. Antimicrobial and anticandidal activities of the extracts and essential oils of Bidens tripartita. Folia Histochem Cyto. 2008;46(3):389–393. doi:10.2478/v10042-008-0082-8, PMid:19056546

Sofowora A. Recent trends in research into African medicinal plants. J Ethnopharmacol. 1993;38(2-3):209–214. doi:10.1016/0378-8741(93)90017-Y

Chingwaru W, Faria ML, Saravia C, Cencic A. Indigenous knowledge of health benefits of marama plant among respondents in Ghantsi and Jwaneng of Botswana. Afr J Food Agric Nutr Dev. 2007;7(6). Available from: http://www.ajfand.net/Issue17/Issue17commentary.htm

Amarteifio J, Moholo D. The chemical composition of four legumes consumed in Botswana. J Food Compos Anal. 1998;11(4):329–332. doi:10.1006/ jfca.1998.0595

Bower N, Hertel K, Storey R, Storey R. Nutritional evaluation of marama bean (Tylosema esculentum, Fabaceae): Analysis of the seed. Econ Bot. 1988;42(4):533–540. doi:10.1007/BF02862798

Keegan AB, Van Staden J. Marama bean, Tylosema esculentum, a plant worthy of cultivation. S Afr J Sci. 1981;77(9):387.

Holse M, Husted S, Hansen A. Chemical composition of marama bean (Tylosema esculentum) – a wild African bean with unexploited potential. J Food Compos Anal. 2010, in press. doi:10.1016/j.jfca.2010.03.006

Dubois M, Lognay G, Baudart E, et al. Chemical characterization of Tylosema-Fassoglensis (Kotschy) Torre and Hillc oilseed. J Sci Food Agric. 1995;67(2):163–167. doi:10.1002/jsfa.2740670204

Francis CM, Campbell MC. New high quality oil seed crops for temperate and tropical Australia. Canberra: Rural Industries Research and Development Corporation; 2003.

Mitei YC, Ngila JC, Yeboah SO, et al. NMR, GC–MS and ESI-FTICR-MS profiling of fatty acids and triacylglycerols in some Botswana seed oils. J Am Oil Chem Soc. 2008;85:1021–1032. doi:10.1007/s11746-008-1301-3

Wehmeyer AS, Lee M, Whiting M. The nutrient composition and dietary importance of some vegetable foods eaten by the !Kung Bushmen. S Afr Med J. 1969;43:1529. PMid:5364781

Gueguen J. Legume seed protein extraction, processing, and end product characteristics. Qual Plant. 1983;32(3-4):267–303. doi:10.1007/BF01091191

Nassar AG, Mubarak AE, El-Beltagy AE. Nutritional potential and functional properties of tempe produced from mixture of different legumes. 1: Chemical composition and nitrogenous constituent. Int J Food Sci Technol. 2008;43(10):1754–1758. doi:10.1111/j.1365-2621.2007.01683.x, PMid:20548306

Belitz HD, Grosch W, Schieberle P. Food chemistry. Berlin: Springer-Verlag, 2004; p. 1070.

Hymowitz T, Collins FI, Walker WM, Walker WM. Relationship between content of oil, protein, and sugar in soybean seed. Agron J. 1972;64(5):613–616. doi:10.2134/agronj1972.00021962006400050019x

Maruatona GN, Duodu KG, Minnaar A. Physicochemical, nutritional and functional properties of marama bean flour. Food Chem. 2010;121(2):400–405. doi:10.1016/j.foodchem.2009.12.054

Ripperger-Suhler JA, Longenecker JB. Assessment of the nutritional value of the marama bean. Report to the Center for the Study of Human Adaptation, Division of Graduate Nutrition, University of Texas, Austin; 1982.

Biesele M, Murray RE. Alternative food plants for arid regions: Marama and other plant foods of Kalahari foragers. An applied ethno-botanical study. Report to the Center for the Study of Human Adaptation, Division of Graduate Nutrition, University of Texas, Austin; 1983.

Parlatan A, Saricoban C, Ozcan MM. Chemical composition and antimicrobial activity of the extracts of Kefe cumin (Laser trilobum L.) fruits from different regions. Int J Food Sci Nutr. 2009;60(7):606–617. doi:10.3109/09637480801993938, PMid:19817640

Mazur W, Fotsis T, Wahala K, et al. Isotope dilution gas chromatographic-mass spectrometric method for the determination of isoflavonoids, coumestrol, and lignans in food samples. Anal Biochem. 1996;233:169–180. doi:10.1006/abio.1996.0025, PMid:8789715

Penalvo JL, Heinonen SM, Nurmi T, et al. Plant lignans in soy-based health supplements. J Agric Food Chem. 2004;52(13):4133–4138. doi:10.1021/jf0497509, PMid:15212459

Kang MS, Oh JS, Kang IC, et al. Inhibitory effect of methyl gallate and gallic acid on oral bacteria. J Microbiol. 2008;46(6):744–750. doi:10.1007/s12275-008- 0235-7, PMid:19107406

O’Dell BL, De Boland A. Complexation of phytate with proteins and cations in corn germ and oilseed meals. J Agric Food Chem. 1976;24(4):804–808. doi:10.1021/jf60206a034

Chang RS, Yeung HW. Inhibition of growth of human immunodeficiency virus in vitro by crude extracts of Chinese medical herbs. Antiviral Res. 1988;9:163–176. doi:10.1016/0166-3542(88)90001-0

Vilhjalmsdottir L, Fisher H. Castor bean meal as a protein source for chickens: Detoxification and determination of limiting amino acids. J Nutr. 1971;101:1185. PMid:5106935

Yu YS, Hsu CL, Yen GC. Anti-inflammatory effects of the roots of Alpinia pricei Hayata and its phenolic compounds. J Agric Food Chem. 2009;57(17):7673–7680. doi:10.1021/jf901327g, PMid:19685877

Krygier K, Sosulski F, Hogge L. Free, esterified, and insoluble-bound phenolic acids. 1. Extraction and purification procedure. J Agric Food Chem. 1982;30:330–334. do doi:10.1021/jf00110a028

Naczk M, Shahidi F. Extraction and analysis of phenolic substances in food. J Chromatogr A. 2004;1054:95–111. doi:10.1016/S0021-9673(04)01409-8, doi:10.1016/j.chroma.2004.08.059, PMid:15553136

BreezeTM. Part number WA01016. Milford, MA: Waters Corporation; 2000.

Kuzina LV, Miller TA, Cooksey DA. In vitro activities of antibiotics and antimicrobial peptides against the plant pathogenic bacterium Xylella fastidiosa. Lett Appl Microbiol. 2006;42:514–520. doi:10.1111/j.1472-765X.2006.01898.x, PMid:16620212

Ali-Shtayeh MS, Yaghmour RM, Faidi YR, et al. Antimicrobial activity of 20 plants used in folkloric medicine in the Palestinian area. J Ethnopharmacol. 1998;60(3):265–271. doi:10.1016/S0378-8741(97)00153-0

National Committee for Clinical Laboratory Standards (NCCLS). Reference method for broth dilution antifungal susceptibility testing of yeasts: Approved Standard M27-A. Wayne, PA: NCCLS; 1997.

Swenson JM, Thornsberry C, Silcos VA. Rapidly growing mycobacteria: Testing of susceptibility to 34 patients. Antimicrob Agents Chemother. 1982;22:186–192. PMid:6927280, PMCid:183707

Zasada AA, Zaleska M, Podlasin RB, Seferynska I. The first case of septicemia due to nontoxigenic Corynebacterium diphtheriae in Poland: Case report. Ann Clin Microbiol Antimicrob. 2005;4:8. doi:10.1186/1476-0711-4-8, PMid:15876349, PMCid:1156865

STATISTICA. Version 7.1. Tulsa, OK: StatSoft Inc.; 2005.

Stermitz FR, Lorenz P, Tawara JN, et al. Synergy in a medicinal plant: Antimicrobial action of berberine potentiated by 5*-methoxyhydnocarpin, a multidrug pump inhibitor. Proc Natl Acad Sci. USA. 2000;97(4):1433–1437. doi:10.1073/pnas.030540597, PMid:10677479

Del Mar C. Urinary tract infections in healthy women: A revolution in management? BMC Fam Pract. 2010;11:42. doi:10.1186/1471-2296-11-42, PMid:20504297, PMCid:2885322

Akinyemi KO, Oluwa OK, Omomigbehin EO. Antimicrobial activity of crude extracts of three medicinal plants used in south-west Nigerian folk medicine on some food borne bacterial pathogens. Afr J Tradit Complement Altern Med. 2006;3(4):13–22.

Cowan MM. Plant products as antimicrobial agents. Clin Microbiol Rev. 1999;12:564–582. PMid:10515903, PMCid:88925

Tian HL, Zhan P, Li KX. Analysis of components and study on antioxidant and antimicrobial activities of oil in apple seeds. Int J Food Sci Nutr. 2010;61(4):395–403. doi:10.3109/09637480903535772, PMid:20128637

Sanchez Perera LM, Varcalcel L, Escobar A, Noa M. Polyphenol and phytosterol composition in an antibacterial extract from Rhizophora mangle L. bark. J Herb Pharmacother. 2007;7(3–4):107–128. PMid:18928137

Kawaguchi Y, Yamauchi S, Masuda K, et al. Antimicrobial activity of stereoisomers of butane-type lignans. Biosci Biotechnol Biochem. 2009;73(8):1806–1810. doi:10.1271/bbb.90167

Akiyama K, Yamauchi S, Maruyama M, et al. Antimicrobial activity of stereoisomers of morinols A and B, tetrahydropyran sesquineolignans. Biosci Biotechnol Biochem. 2009;73(1):129–133. doi:10.1271/bbb.80536

Nakato T, Yamauchi S, Tago R, et al. Syntheses and antimicrobial activity of tetrasubstituted tetrahydrofuran lignan stereoisomers. Biosci Biotechnol Biochem. 2009;73(7):1608–1617. doi:10.1271/bbb.90107

Rijo P, Simoes MF, Duarte A, Rodriguez B. Isopimarane diterpenoids from Aeollanthus rydingianus and their antimicrobial activity. Phytochemistry. 2009;70(9):1161–1165. doi:10.1016/j.phytochem.2009.06.008, PMid: 19631355

Nadaraja D, Weintraub ST, Hakala KW, et al. Isolation and partial sequence of a Kunitz-type elastase specific inhibitor from marama bean (Tylosema esculentum). J Enzyme Inhib Med Chem. 2010;25(3):377–382. doi:10.3109/14756360903179500, PMid:19883219

Brown SE, Howard A, Kasprzak AB, et al. A peptidomics study reveals the impressive antimicrobial peptide arsenal of the wax moth Galleria mellonella. Insect Biochem Mol Biol. 2009;39(11):792–800. doi:10.1016/j.ibmb.2009.09.004, PMid:19786100



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