Abstract
Bacteria are increasingly resistant to common antibiotics. Certain fatty acids are effective antibacterial agents and, when compared to conventional antibiotics, have fewer incidences of bacterial resistance. Algae naturally synthesize these fatty acids and can provide a sustainable source of these antibiotics. To evaluate the antibacterial properties of fatty acids, 29 acids present in algae were tested for topical antibacterial properties on Escherichia coli and Staphylococcus aureus using surface zone inhibition assay. From the set of fatty acids showing good antibacterial activity, five representative fatty acids—capric acid (10:0), palmitoleic acid (16:1), gamma-linolenic acid [18:3 (n-6)], arachidonic acid [20:4 (n-6)], and docosadienoic acid [22:2 (n-6)]—were selected for further analysis. Algal growth conditions (light, temperature, and nutrients) were manipulated to increase the content of the selected target fatty acids in five algal species (Rhodella maculata, Phaeodactylum tricornutum, Boekelovia hooglandii, Goniochloris sculpta, and Chloridella simplex). P. tricornutum contained the highest content of the target antibacterial fatty acids, with a maximum of 206 mg g−1 dry weight (dw). However, biomass productivity was low; thus, for commercial viability, initial growth should be under optimum conditions and then shifted to enhance antibacterial fatty acid content. B . hooglandii had the highest biomass productivity and a total antibacterial fatty acid content of 32.6 mg g−1 dw in Erddekokt + Salze + Peptone (ESP) medium, 18 °C, 80 μmol photons m−2 s−1, and 17:7-h light/dark cycle. This study identifies fatty acids that have effective antibacterial properties and potential use as topical antibacterial products and determined growth conditions that result in algae rich in these acids.
Similar content being viewed by others
References
Andersen RA (ed) (2005) Algal culturing techniques. Elsevier Academic Press, New York, 578 pp
Clinical and Laboratory Standards Institute (2006) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard-seventh edition, 7th edn. Clinical and Laboratory Standards Institute, Wayne, Pennsylvania
Dawson PL, Carl GD, Acton JC, Han IY (2002) Effect of lauric acid and nisin-impregnated soy-based films on the growth of Listeria monocytogenes on turkey bologna. Poult Sci 81:721–726
Desbois AP, Smith VJ (2010) Antibacterial free fatty acids: activities, mechanisms of action and biotechnological potential. Appl Microbiol Biotechnol 85:1629–1642
Desbois AP, Mearns-spragg A, Smith VJ (2009) A fatty acid from the diatom Phaeodactylum tricornutum is antibacterial against diverse bacteria including multi-resistant Staphylococcus aureus (MRSA). Mar Biotechnol 11:45–52
Experimental Phycology and Culture Collection of Algae (SAG) (2014) List of media and recipes. http://www.uni-goettingen.de/en/list-of-media-and-recipes/186449.html. Accessed 5 June 2014
Findlay JA, Patil AD (1984) Antibacterial constituents of the diatom Navicula delognei. J Nat Prod 47:815–818
Galbraith H, Miller TB, Paton AM, Thompson JK (1971) Antibacterial activity of long chain fatty acids and the reversal with calcium, magnesium, ergocalciferol and cholesterol. J Appl Bacteriol 34:803–813
Gong Y, Hu H, Gao Y, Xu X, Gao H (2011) Microalgae as platforms for production of recombinant proteins and valuable compounds: progress and prospects. J Ind Microbiol Biotechnol 38:1879–1890
Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 29–60
Guschina and Harwood (2009) Algal lipids and effect of the environment on their biochemistry. In: Arts MT, Brett MT, Kainz M (eds) Lipids in aquatic ecosystems. Springer, NY, pp 1–24
Heman-Ackah SH (1976) Comparison of tetracycline action of Staphylococcus aureus and Escherichia coli by microbial kinetics. Antimicrob Agents Chemother 10:223–228
Hu Q (2007) Environmental effects on cell composition. In: Richmond A (ed) Handbook of microalgal culture: biotechnology and applied phycology. Blackwell Publishing Ltd., Oxford, pp 83–95
Huang H, Xiao X, Shi J, Chen Y (2014) Structure–activity analysis of harmful algae inhibition by congeneric compounds: case studies of fatty acids and thiazolidinediones. Environ Sci Pollut Res. doi:10.1007/s11356-014-2626-0:1-11
Jones J, Lee C-H, Wang J, Poenie M (2012) Use of anion exchange resins for one-step processing of algae from harvest to biofuel. Energies 5:2608–2625
Jüttner F (2001) Liberation of 5, 8, 11, 14, 17-eicosapentaenoic acid and other polyunsaturated fatty acids from lipids as a grazer defense reaction in epilithic diatom biofilms. J Phycol 37:744–755
Kabara JJ, Swieczkowski DM, Conley AJ, Truant JP (1972) Fatty acids and derivatives as antimicrobial agents. Antimicrob Agents Chemother 2:23–23
Katsuta Y, Iida T, Inomata S, Denda M (2005) Unsaturated fatty acids induce calcium influx into keratinocytes and cause abnormal differentiation of epidermis. J Investig Dermatol 124:1008–1013
Lang I, Hodac L, Friedl T, Feussner I (2011) Fatty acid profiles and their distribution patterns in microalgae: a comprehensive analysis of more than 2000 strains from the SAG culture collection. BMC Plant Biol 11:124
Metherel AH, Aristizabal Henao JJ, Stark KD (2013) EPA and DHA levels in whole blood decrease more rapidly when stored at −20°C as compared with room temperature, 4 and −75°C. Lipids 48:1079–1091
Nagaraja TG (1995) Ionophores and antibiotics in ruminants. In: Wallace RJ, Chesson A (eds) Biotechnology in animal feeds and animal feeding. Wiley-VCH Verlag GmbH, Weinheim, pp 173–204
Naviner M, Berge J-P, Durand P, Bris HL (1999) Antibacterial activity of the marine diatom Skeletonema costatum against aquacultural pathogens. Aquaculture 174:15–24
Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47:541–568
Ohta S, Chang T, Kawashima A, Nagate T, Murase M, Nakanishi H, Miyata H, Kondo M (1994) Anti methicillin-resistant Staphylococcus aureus (MRSA) activity by linolenic acid isolated from the marine microalga Chlorococcum HS-101. Bull Environ Contam Toxicol 52:673–680
Petschow BW, Batema RP, Ford LL (1996) Susceptibility of Helicobacter pylori to bactericidal properties of medium-chain monoglycerides and free fatty acids. Antimicrob Agents Chemother 40:302–306
Pratt R (1942) Studies on Chlorella vulgaris. V. Some properties of the growth-inhibitor formed by Chlorella cells. Am J Bot 29:142–148
Royce LA, Liu P, Stebbins MJ, Hanson BC, Jarboe LR (2013) The damaging effects of short chain fatty acids on Escherichia coli membranes. Appl Microbiol Biotechnol 97:8317–8327
Ruffell SE, McConkey BJ, Müller KM (2015) Omega-3 fatty acid profiles and growth of five algae for potential use in industrial applications. J Appl Phycol (submitted)
Russel AD (1991) Mechanisms of bacterial resistance to non-antibiotics: food additives and food pharmaceutical preservatives. J Appl Bacteriol 71:191–201
Sader HS, Ferraro MJ, Reller LB, Schreckenberger PC, Swenson JM, Jones RN (2007) Reevaluation of Clinical and Laboratory Standards Institute disk diffusion breakpoints for tetracyclines for testing Enterobacteriaceae. J Clin Microbiol 45:1640–1640
Sheehan J, Dunahay T, Benemann J, Roessler P (1998) A look back at the U.S. Department of Energy’s Aquatic Species Program—biodiesel from algae. Laboratory NRE, Golden, Colorado. NREL/TP-580-24190
Stein JR (1980) Handbook of phycological methods: culture methods and growth measurements. Cambridge University Press, Cambridge, p 472
Sukenik A, Carmeli Y (1990) Lipid synthesis and fatty acid composition in Nannochloropsis sp. (Eustigmatophyceae) grown in a light–dark cycle. J Phycol 26:463–469
Sun CQ, O’Connor CJ, Roberton AM (2003) Antibacterial actions of fatty acids and monoglycerides against Helicobacter pylori. FEMS Immunol Med Microbiol 36:9–17
Sussman M (1997) Escherichia coli and human disease. In: Sussman M (ed) Escherichia coli mechanisms of virulence. University Press, Cambridge, pp 3–48
Wada H, Murata N (2009) Lipids in photosynthesis: essential and regulatory functions. Springer, Dordrecht, pp 144–244
Yongmanitchai W (1991) Production of eicosapentaenoic acid from a freshwater diatom, Phaeodactylum tricornutum. PhD Thesis, University of Waterloo, Canada
Yongmanitchai W, Ward OP (1991) Growth of and omega-3 fatty acid production by Phaeodactylum tricornutum under different culture conditions. Appl Environ Microbiol 57:419–425
Zuñiga PK, Ciobanu FA, Nuñeza OM, Stark KD (2012) The use of direct transesterification methods and autoclaving for determining fatty acid yields from dried Philippine thraustochytrids, a potential source of docosahexaenoic acid. J Funct Foods 4:915–923
Acknowledgments
We are extremely grateful to Ms. S. Vesely, at the University of Waterloo, for her technical support throughout the experiment. In addition, we thank Dr. Laura Dindia and Ms. Maricor Arlos for their constructive comments. This research was funded by NSERC discovery grants to KMM and BJM as well as a FedDev Ontario ARC grant (Applied Research and Commercialization Initiative) to KMM and BJM and matching ARC support from Algae Dynamics.
Conflict of interest
The authors declare no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ruffell, S.E., Müller, K.M. & McConkey, B.J. Comparative assessment of microalgal fatty acids as topical antibiotics. J Appl Phycol 28, 1695–1704 (2016). https://doi.org/10.1007/s10811-015-0692-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-015-0692-4