Effect of green alga Planktochlorella nurekis on selected bacteria revealed antibacterial activity in vitro
L. Čermák, Š. Pražáková, M. Marounek, M. Skřivan, E. Skřivanováhttps://doi.org/10.17221/8522-CJASCitation:Čermák L., Pražáková Š., Marounek M., Skřivan M., Skřivanová E. (2015): Effect of green alga Planktochlorella nurekis on selected bacteria revealed antibacterial activity in vitro . Czech J. Anim. Sci., 60: 427-435.
The green alga Planktochlorella nurekis (Chlorellaceae, Chlorophyta) is considered a producer of antibacterial mixture of long-chain fatty acids, which has possibly similar composition and mode of action as chlorellin produced by another green alga, Chlorella vulgaris. Although the antibacterial properties of C. vulgaris have been reported, the interactions of P. nurekis with bacteria have not been determined yet. The aim of this study was to elucidate the effect of P. nurekis water suspension on growth of selected gastrointestinal bacteria in vitro so that it could be used as a suitable feed supplement in animal farming. Unknown bacterial populations occurring in the algal suspension were identified using 16S rRNA sequencing assay. Selected strains were cultivated with lyophilized P. nurekis and the antibacterial effect was monitored. The composition of fatty acids and heat sensitivity of antibacterial substances were also examined. Sequencing analysis of 71 bacterial 16S rRNA genes in xenic algal suspension identified common environmental microbiota, one strain belonging to the class Alphaproteobacteria, 17 to Betaproteobacteria, 44 to Gammaproteobacteria (dominated by Pseudomonas putida strains), and nine to Sphingobacteria. The antimicrobial activity of P. nurekis suspension was tested at a concentration range of 0.75–6 mg/ml. The highest inhibitory effect was observed on bifidobacteria. Statistically significant reductions in bacterial counts were also observed for Escherichia coli, Salmonella enterica var. Enteritidis, S. enterica var. Infantis, Campylobacter jejuni, and Arcobacter butzleri. The growth of Lactobacillus johnsonii was significantly stimulated. The relative proportions of C14–C22 fatty acids in P. nurekis were found as follows: saturated 54.28%, monounsaturated 30.40%, and polyunsaturated 7.16%. The antibacterial compounds present in P. nurekis suspension exhibited thermostability. The results indicate that P. nurekis can inhibit some pathogenic gastrointestinal bacteria and seems to be a promising essential nutrients source in animal nutrition.Keywords:chlorellin; fatty acids; gastrointestinal bacteria; interaction; microalgae; thermostabilityReferences:
Abdel-Baki A.S., Dkhil M.A., Al-Quraishy S. (2011): Bioaccumulation of some heavy metals in tilapia fish relevant to their concentration in water and sediment of Wadi Hanifah, Saudi Arabia. African Journal of Biotechnology, 10, 2541–2547.Agemian Haig, Sturtevant D. P., Austen K. D. (1980): Simultaneous acid extraction of six trace metals from fish tissue by hot-block digestion and determination by atomic-absorption spectrometry. The Analyst, 105, 125- https://doi.org/10.1039/an9800500125Alves L. C., Glover C. N., Wood C. M. (2006): Dietary Pb Accumulation in Juvenile Freshwater Rainbow Trout (Oncorhynchus mykiss). Archives of Environmental Contamination and Toxicology, 51, 615-625 https://doi.org/10.1007/s00244-005-0212-7Bergman H.L., Dorward-King E.J. (1997): Reassessment of metals criteria for aquatic life protection. SETAC Press, Pensacola, USA.Boyd Robert S. (2010): Heavy Metal Pollutants and Chemical Ecology: Exploring New Frontiers. Journal of Chemical Ecology, 36, 46-58 https://doi.org/10.1007/s10886-009-9730-5Carmouche Jonathan J., Puzas J. Edward, Zhang Xinping, Tiyapatanaputi Prarop, Cory-Slechta Deborah A., Gelein Robert, Zuscik Michael, Rosier Randy N., Boyce Brendan F., O’Keefe Regis J., Schwarz Edward M. (2005): Lead Exposure Inhibits Fracture Healing and Is Associated with Increased Chondrogenesis, Delay in Cartilage Mineralization, and a Decrease in Osteoprogenitor Frequency. Environmental Health Perspectives, 113, 749-755 https://doi.org/10.1289/ehp.7596Commission Regulation (EC) No. 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Official Journal of the European Union, L364, 5–24.Eyckmans Marleen, Lardon Isabelle, Wood Chris M., De Boeck Gudrun (2013): Physiological effects of waterborne lead exposure in spiny dogfish (Squalus acanthias). Aquatic Toxicology, 126, 373-381 https://doi.org/10.1016/j.aquatox.2012.09.004George K.R., Malini N.A., Rajan A., Deepa R. (2011): Enzymatic changes in the kidney and brain of freshwater murrel, Channa striatus (Bloch) on short term exposure to sub-lethal concentration of lead nitrate. Indian Journal of Fisheries, 58, 91–94.Heath A.G. (ed.) (1995): Water Pollution and Fish Physiology. CRC Press, Boca Raton, USA.Iavicoli I., Carelli G., Stanek E.J., Castellino N., Li Z., Calabrese E.J. (2006): Low doses of dietary lead are associated with a profound reduction in the time to the onset of puberty in female mice. Reproductive Toxicology, 22, 586-590 https://doi.org/10.1016/j.reprotox.2006.03.016Jumawan J.C., Salunga T.P., Catap E.S. (2010): Lipid peroxidation and patterns of cadmium and lead accumulation in the vital organs of the Suckermouth armored catfish Pterygoplichthys Gill, 1858 from Marikina River, Philippines. Journal of Applied Sciences in Environmental Sanitation, 5, 375–390.Kah O. (1989): Development of an enzyme-linked immunosorbent assay for goldfish gonadotropin. Biology of Reproduction, 41, 68-73 https://doi.org/10.1095/biolreprod41.1.68Khan I.A, Thomas P (2000): Lead and Aroclor 1254 disrupt reproductive neuroendocrine function in Atlantic croaker. Marine Environmental Research, 50, 119-123 https://doi.org/10.1016/S0141-1136(00)00108-2Kleinow K.M., James M.O. (2001): Response of the teleost gastrointestinal system to xenobiotics. In: Schlenk D. and Benson W.H. (eds): Target Organ Toxicity in Marine and Freshwater Teleosts. Vol. 1 – Organs. Taylor & Francis, London, UK, 269–362.Kwon S.Y., Bae O.N., Noh J.Y., Kim K., Kang S., Shin Y.J., Lim K.M., Chung J.H. (2015): Erythrophagocytosis of lead-exposed erythrocytes by renal tubular cells: possible role in lead-induced nephrotoxicity. Environmental Health Perspectives, 123, 120–127.Lucchi L., Memo M., Airaghi M.L., Spano P.F., Trabucchi M. (1981): Chronic lead treatment induces in rat a specific and differential effect on dopamine receptors in different brain areas. Brain Research, 213, 397-404 https://doi.org/10.1016/0006-8993(81)90244-4Łuszczek-Trojnar Ewa, Drąg-Kozak Ewa, Popek Włodzimierz (2013): Lead accumulation and elimination in tissues of Prussian carp, Carassius gibelio (Bloch, 1782), after long-term dietary exposure, and depuration periods. Environmental Science and Pollution Research, 20, 3122-3132 https://doi.org/10.1007/s11356-012-1210-8Łuszczek-Trojnar Ewa, Drąg-Kozak Ewa, Szczerbik Paweł, Socha Magdalena, Popek Włodzimierz (2014): Effect of long-term dietary lead exposure on some maturation and reproductive parameters of a female Prussian carp (Carassius gibelio B.). Environmental Science and Pollution Research, 21, 2465-2478 https://doi.org/10.1007/s11356-013-2184-xMager E.M. (2011): Lead. In: Wood C.M., Farrell A.P., Brauner C.J. (eds): Homeostasis and Toxicology of Non-essential Metals. Fish Physiology. Academic Press, New York, USA, 185–236.Mager Edward M., Brix Kevin V., Grosell Martin (2010): Influence of bicarbonate and humic acid on effects of chronic waterborne lead exposure to the fathead minnow (Pimephales promelas). Aquatic Toxicology, 96, 135-144 https://doi.org/10.1016/j.aquatox.2009.10.012Mager Edward M., Brix Kevin V., Gerdes Robert M., Ryan Adam C., Grosell Martin (2011): Effects of water chemistry on the chronic toxicity of lead to the cladoceran, Ceriodaphnia dubia. Ecotoxicology and Environmental Safety, 74, 238-243 https://doi.org/10.1016/j.ecoenv.2010.11.005Mebane Christopher A., Hennessy Daniel P., Dillon Frank S. (2008): Developing Acute-to-chronic Toxicity Ratios for Lead, Cadmium, and Zinc using Rainbow Trout, a Mayfly, and a Midge. Water, Air, and Soil Pollution, 188, 41-66 https://doi.org/10.1007/s11270-007-9524-8Mobarak Y.M. (2008): Review of the developmental toxicity and teratogenicity of three environmental contaminants (cadmium, lead and mercury). Catrina, 3, 31–43.Mobarak Yomn Mohamed Shahat, Sharaf Mariam Mahmoud (2011): Lead Acetate-induced Histopathological Changes in the Gills and Digestive System of Silver Sailfin Molly (Poecilia latipinna). International Journal of Zoological Research, 7, 1-18 https://doi.org/10.3923/ijzr.2011.1.18Mount David R., Barth Anita K., Garrison Tyler D., Barten Karen A., Hockett J. Russell (1994): DIETARY AND WATERBORNE EXPOSURE OF RAINBOW TROUT (ONCORHYNCHUS MYKISS) TO COPPER, CADMIUM, LEAD AND ZINC USING A LIVE DIET. Environmental Toxicology and Chemistry, 13, 2031- https://doi.org/10.1897/1552-8618(1994)13[2031:DAWEOR]2.0.CO;2Muñoz Lautaro, Weber Paula, Dressler Valderi, Baldisserotto Bernardo, Vigliano Fabricio Andrés (2015): Histopathological biomarkers in juvenile silver catfish (Rhamdia quelen) exposed to a sublethal lead concentration. Ecotoxicology and Environmental Safety, 113, 241-247 https://doi.org/10.1016/j.ecoenv.2014.11.036Ojo Adeola A., Wood Chris M. (2007): In vitro analysis of the bioavailability of six metals via the gastro-intestinal tract of the rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology, 83, 10-23 https://doi.org/10.1016/j.aquatox.2007.03.006Persson P., Bjornsson B. Th., Takagi Y. (1999): Characterization of morphology and physiological actions of scale osteoclasts in the rainbow trout. Journal of Fish Biology, 54, 669-684 https://doi.org/10.1111/j.1095-8649.1999.tb00645.xPounds J G, Long G J, Rosen J F (1991): Cellular and molecular toxicity of lead in bone. Environmental Health Perspectives, 91, 17-32 https://doi.org/10.1289/ehp.919117Rabinowitz M B (1991): Toxicokinetics of bone lead. Environmental Health Perspectives, 91, 33-37 https://doi.org/10.1289/ehp.919133Rademacher David J., Steinpreis Rhea E., Weber Daniel N. (2003): Effects of dietary lead and/or dimercaptosuccinic acid exposure on regional serotonin and serotonin metabolite content in rainbow trout (Oncorhynchus mykiss). Neuroscience Letters, 339, 156-160 https://doi.org/10.1016/S0304-3940(03)00013-2Reichert William L., Federighi David A., Malins Donald C. (1979): Uptake and metabolism of lead and cadmium in Coho salmon (oncorhynchus kisutch). Comparative Biochemistry and Physiology Part C: Comparative Pharmacology, 63, 229-234 https://doi.org/10.1016/0306-4492(79)90066-2Ruby S. M., Hull R., Anderson P. (2000): Sublethal Lead Affects Pituitary Function of Rainbow Trout During Exogenous Vitellogenesis. Archives of Environmental Contamination and Toxicology, 38, 46-51 https://doi.org/10.1007/s002449910006Scott G. R. (): Cadmium disrupts behavioural and physiological responses to alarm substance in juvenile rainbow trout (Oncorhynchus mykiss). Journal of Experimental Biology, 206, 1779-1790 https://doi.org/10.1242/jeb.00353Sadhana Sharma (2011): Lead toxicity, oxidative damage and health implications. A review. International Journal for Biotechnology and Molecular Biology Research, 2, - https://doi.org/10.5897/IJBMBRX11.002Siscar R., Torreblanca A., Palanques A., Solé M. (2013): Metal concentrations and detoxification mechanisms in Solea solea and Solea senegalensis from NW Mediterranean fishing grounds. Marine Pollution Bulletin, 77, 90-99 https://doi.org/10.1016/j.marpolbul.2013.10.026Sloman Katherine A., Lepage Olivier, Rogers Joseph T., Wood Chris M., Winberg Svante (2005): Socially-mediated differences in brain monoamines in rainbow trout: effects of trace metal contaminants. Aquatic Toxicology, 71, 237-247 https://doi.org/10.1016/j.aquatox.2004.11.008Spieler R.E., Russo A.C., Weber D.N. (1995): Waterborne lead affects circadian variations of brain neurotransmitters in fathead minnows. Bulletin of Environmental Contamination and Toxicology, 55, - https://doi.org/10.1007/BF00206680Steuerwald Amy J., Blaisdell Frank S., Geraghty Ciaran M., Parsons Patrick J. (): Regional Distribution and Accumulation of Lead in Caprine Brain Tissues Following a Long-Term Oral Dosing Regimen. Journal of Toxicology and Environmental Health, Part A, 77, 663-678 https://doi.org/10.1080/15287394.2014.880328Thomas Peter (1988): Reproductive endocrine function in female atlantic croaker exposed to pollutants. Marine Environmental Research, 24, 179-183 https://doi.org/10.1016/0141-1136(88)90294-2Varanasi Usah, Gmur Dennis J. (1978): Influence of water-borne and dietary calcium on uptake and retention of lead by coho salmon (Oncorhynchus kisutch). Toxicology and Applied Pharmacology, 46, 65-75 https://doi.org/10.1016/0041-008X(78)90137-0Weber D.N. (1993): Exposure to sublethal levels of waterborne lead alters reproductive behavior patterns in fathead minnows (Pimephales promelas). Neurotoxicology, 14, 347–358.Weis Judith S, Samson Jennifer, Zhou Tong, Skurnick Joan, Weis Peddrick (2003): Evaluating prey capture by larval mummichogs (Fundulus heteroclitus) as a potential biomarker for contaminants. Marine Environmental Research, 55, 27-38 https://doi.org/10.1016/S0141-1136(02)00204-0Woodward Daniel F., Brumbaugh William G., Delonay Aaron J., Little Edward E., Smith Charlie E. (1994): Effects on Rainbow Trout Fry of a Metals-Contaminated Diet of Benthic Invertebrates from the Clark Fork River, Montana. Transactions of the American Fisheries Society, 123, 51-62 https://doi.org/10.1577/1548-8659(1994)123<0051:EORTFO>2.3.CO;2