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Inhibition of pathogenic Vibrio by the microalgae Isochrysis galbana

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Abstract

Vibrio alginolyticus, Vibrio campbellii, and Vibrio harveyi were inhibited by Isochrysis galbana in batch cultures. I. galbana reduced the V. alginolyticus, V. campbellii, and V. harveyi counts to undetectable levels in 2, 4, and 7 days (<0.01 Vibrio spp. mL−1), respectively, remaining so until the end of the experiment on day 15. Other heterotrophic bacteria reached counts of 106 CFU mL−1 on ZoBell medium at the end of the experiment. Vibrio parahaemolyticus was not inhibited by I. galbana. In all mixed I. galbana and Vibrio spp. cultures, the algal density increased from 3.5 to 4.0 × 107 cells mL−1, higher than that in I. galbana cultures alone, indicating a lack of an inhibitory effect on microalgae in the mixed cultures. The predominant fatty acids (>82 %) of I. galbana during the stationary growth phase were estearidonic (24.3 %), oleic (15.7 %), myristic (13.8 %), docosahexaenoic (11.0 %), palmitic (10.3 %), and α-linolenic (7.2 %) acids. These results demonstrate that I. galbana synthesizes antibacterial fatty acids that inhibit the growth of pathogenic bacteria such as V. alginolyticus, V. campbellii, and V. harveyi.

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References

  • Anguiano-Beltrán C, Searcy-Bernal R, Lizárraga-Partida ML (1998) Pathogenic effects of Vibrio alginolyticus on larvae and postlarvae of the red abalone Haliotis rufescens. Dis Aquat Org 33:119–122

    Article  Google Scholar 

  • Anguiano-Beltrán C, Lizárraga-Partida ML, Searcy-Bernal R (2004) Effect of Vibrio alginolyticus on larval survival of the blue mussel Mytilus galloproviciallis. Dis Aquat Org 59:119–123

    Article  PubMed  Google Scholar 

  • Austin B, Day JG (1990) Inhibition of prawn pathogenic Vibrio spp. by a commercial spray-dried preparation of Tetraselmis suecica. Aquaculture 90:389–392

    Article  Google Scholar 

  • Austin B, Baudet E, Stobie M (1992) Inhibition of bacterial fish pathogens by Tetraselmis suecica. J Fish Dis 15:55–61

    Article  Google Scholar 

  • Austin B, Austin DA, Farhat Z, Robertson PAW (1999) Diagnosis and control of bacterial fish pathogens with emphasis on Vibrio harveyi. J Ocean Univ Quingdao 29:489–499

    CAS  Google Scholar 

  • Banerjee S, Chen Ooi M, Shariff M, Khatoon H (2012) Antibiotic resistant Salmonella and Vibrio associated with farmed Litopenaeus vannamei. Sci World J 2012:130–136

    Article  Google Scholar 

  • Borowitzka MA (1995) Microalgae as sources of pharmaceuticals and others biologically active compounds. J Appl Phycol 7:3–15

    Article  CAS  Google Scholar 

  • Bougaran G, Le Déan LL, Lukomska E, Kaas R, Baron R (2003) Transient initial phase in continuous culture of Isochrysis galbana affinis Tahiti. Aquat Living Resour 16:389–394

    Article  Google Scholar 

  • Brown MR (2002) Nutritional value of microalgae for aquaculture. In: Cruz-Suárez LE, Ricque-Marie D, Tapia-Salazar M, Gaxiola-Cortez MG, Simoes N (eds) Avances en Nutrición Acuícola. VI Simposium Internacional de Nutrición Acuícola. Cancún, Quintana Roo, México, pp 281–292

    Google Scholar 

  • Bruce DL, Duff DCB, Antia NJ (1967) The identification of two antibacterial products of the marine planktonic alga Isochrysis galbana. J Gen Microbiol 48:293–298

    Article  CAS  PubMed  Google Scholar 

  • Cabello FC (2006) Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol 8:1137–1144

    Article  CAS  PubMed  Google Scholar 

  • Campa-Córdova AI, Luna-González A, Ascencio F, Cortéz-Jacinto E, Cáceres-Martínez CJ (2006) Effects of chloramphenicol, erytromicin, and furazolidone on the growth of Isochrysis galbana and Chaetoceros gracilis. Aquaculture 260:145–150

    Article  Google Scholar 

  • Chen W, Li CH, Chen JC (2004a) Effect of dissolved oxygen on the immune response of Haliotis diversicolor supertexta and its susceptibility to Vibrio parahaemolyticus. Aquaculture 232:103–115

    Article  Google Scholar 

  • Chen W, Hsiao IS, Chen JC (2004b) Effect of ammonia on the immune response of Taiwan Haliotis diversicolor supertexta and its susceptibility to Vibrio parahaemolyticus. Fish Shellfish Immun 17:193–202

    Article  CAS  Google Scholar 

  • Chen W, Hsiao IS, Chen JC (2004c) Change in water temperature on the immune response of Taiwan Haliotis diversicolor supertexta and its susceptibility to Vibrio parahaemolyticus. Fish Shellfish Immun 17:235–243

    Article  Google Scholar 

  • Defoirdt T, Boon N, Boisser P, Verstraete W (2004) Disruption of bacterial quorum sensing: an unexplored strategy to fight infections in aquaculture. Aquaculture 240:69–88

    Article  Google Scholar 

  • Defoirdt T, Crab R, Wood T, Sorgeloos P, Verstraete W, Bossier P (2006) Quorum sensing-disrupting brominated furanones protect the gnotobiotic brine shrimp Artemia franciscana from pathogenic Vibrio harveyi, Vibrio campbellii, and Vibrio parahaemolyticus isolates. Appl Environ Microbiol 72:6419–6423

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Defoirdt T, Sorgeloos P, Bossier P (2011) Alternatives to antibiotics for the control of bacterial diseases in aquaculture. Curr Opin Microbiol 14:251–258

    Article  PubMed  Google Scholar 

  • Desbois AP, Lebl T, Yan L, Smith V (2008) Isolation and structural characterization of two antibacterial free fatty acids from the marine diatom, Phaeodactylum tricornutum. Appl Mar Biotechnol 81:755–764

    Article  CAS  Google Scholar 

  • Desbois AP, Smith VJ (2010) Antibacterial free fatty acids: activities, mechanisms of action and biotechnological potential. Appl Microbiol Biotechnol 85:1626–1642

    Article  Google Scholar 

  • Douillet P, Langdon Ch J (1994) Use of a probiotic for the culture of larvae of the Pacific oyster (Crassostrea gigas Thunberg). Aquaculture 119:25–40

    Article  Google Scholar 

  • Duff DC, Bruce DL, Antia NJ (1966) The antibacterial activity of marine planktonic algae. Can J Microbiol 12:878–884

    Article  Google Scholar 

  • Fábregas J, García D, Fernández AM, Rocha AL, Gómez P, Escribano JM, Otero A, Coll JM (1999) In vitro inhibition of replication of septicemia virus (VHS) and African swine fever virus (ASFV) by extracts from marine microalgae. Antiviral Res 44:67–73

    Article  PubMed  Google Scholar 

  • Fogg GE, Thake BJ (1987) Algal cultures and phytoplankton ecology. University of Wisconsin Press, London, p 269

    Google Scholar 

  • Folch J, Lee M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissue. J Biol Chem 22:477–509

    Google Scholar 

  • Gauger EJ, Gómez-Chiarri M (2002) 16S ribosomal sequencing confirms the synonym of Vibrio harveyi and V. carchariae. Dis Aquat Org 52:39–46

    Article  CAS  PubMed  Google Scholar 

  • Gómez-Gil B, Thomson FL, Thompson CC, García-Gasca A, Roque A, Swing J (2004) Vibrio hispanicus sp. nov. isolated from Artemia sp. and sea water in Spain. Int J Syst Evol Microbiol 54:261–265

    Article  PubMed  Google Scholar 

  • González-Davis O, Ponce-Rivas E, Sánchez-Saavedra MP, Muñoz-Márquez E, Gerwick W (2012) Bioprospection of microalgae and cyanobacteria as biocontrol agents against Vibrio campbellii and their use in white shrimp Litopenaeus vannamei culture. J World Aquacult Soc 43:387–399

    Article  Google Scholar 

  • Guillard RLL, Ryther JH (1962) Studies on marine planktonic diatoms: I. Cyclotella nana Hustedt and Detenula confervacea (Cleve) Gran. Can J Microbiol 8:229–239

    Article  CAS  PubMed  Google Scholar 

  • Haldar S, Chatterjee S, Sugimoto N, Das S, Chowdhury N, Hinemoya A, Asakura M, Yamasaki S (2011) Identification of Vibrio campbellii isolated from diseased farm shrimp south India and establishing its pathogenic potential in Artemia model. Microbiology 157:179–188

    Article  CAS  PubMed  Google Scholar 

  • Imada N, Kobayashi K, Isdmura K, Saito H, Imura S, Tahara K, Oshima Y (1992) Isolation and identification of an autoinhibitor produced by Skeletonema costatum. Nippon Suisan Gakkaishi 58:1687–1692

    Article  Google Scholar 

  • Immanuel G, Vincybai VC, Sivaram V, Palavesam A, Marian MP (2004) Effect of butanolic extracts from terrestrial herbs and seaweeds on the survival, growth and pathogen (Vibrio parahemolyticus) load on shrimp Penaeus indicus juveniles. Aquaculture 236:53–65

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Karunasagar I, Pai R, Malati GR, Karunasagar I (1994) Mass mortality of Penaeus monodon larvae due to antibiotic-resistant Vibrio harveyi infection. Aquaculture 128:203–209

    Article  Google Scholar 

  • Kim SK, Nonaka L, Suzuki S (2004) Occurrence of tetracycline resistance genes tet (M) and tet (S) in bacteria from marine aquaculture sites. FEMS Microbiol Lett 237:147–156

    Article  CAS  PubMed  Google Scholar 

  • Kokou F, Makridis P, Kentouri M, Divanach P (2012) Antibacterial activity in microalgae cultures. Aquac Res 43:1520–1527

    Article  Google Scholar 

  • Lin W, Chen D, Liu XY (2000) Growth feature of vibrios in microalgae culture systems. Oceanol Limnol Sin 31:4

    Google Scholar 

  • Lin YH, Chang FL, Tsao C-Y, Leu JY (2007) Influence of growth phase and nutrient source on fatty acid composition of Isochrysis galbana CCMP 1324 in a batch photoreactor. Biochem Eng J 37:166–176

    Article  CAS  Google Scholar 

  • Liu CP, Lin LP (2001) Ultrastructural study and lipid formation of Isochrysis sp. CCMP 1324. Bot Bull Acad Sin 42:207–214

    CAS  Google Scholar 

  • Liu PC, Chuang WH, Lee KK (2003) Infectious gastroenteritis caused by V. harveyi (V. carchariae) in cultured red drum, Sciaenops ocellatus. J Appl Ichthyol 19:59–61

    Article  Google Scholar 

  • Lizárraga-Partida ML, Montoya-Rodríguez L, Gendrop-Funes V (1997) The use of bacterial counts in two Mexican shrimp hatcheries. Cienc Mar 23:129–140

    Google Scholar 

  • López-Alonso M-GE, Sánchez-Pérez JA, García-Sánchez JL, García-Camacho F (1991) Fatty acid variation among different isolates of a single strain of Isochrysis galbana. Phytochemistry 31:3901–3904

    Article  Google Scholar 

  • López-Torres MA, Lizárraga-Partida ML (2001) Bacteria isolated on TCBS media associated with hatched Artemia cysts of commercial brands. Aquaculture 194:11–20

    Article  Google Scholar 

  • Maeda M, Nogami K, Kanematsu M, Hirayama K (1997) The concept of biological control in aquaculture. Hydrobiologia 358:285–290

    Article  Google Scholar 

  • Makridis P, Alves Costa R, Dinis MT (2006) Microbial conditions and antimicrobial activity in cultures of two microalga species, Tetraselmis chuii and Chlorella minutissima, and effect on bacterial load of enriched Artemia metanauplii. Aquaculture 255:76–81

    Article  Google Scholar 

  • Marshall JA, Ross T, Pyecroft S, Hallegraeff G (2005) Superoxide production by marine microalgae. Mar Biol 147:541–549

    Article  CAS  Google Scholar 

  • Metcalfe LD, Schmitz AA, Pelka JR (1966) Rapid preparation of fatty acid esters from lipids for gas chromatographic analysis. Anal Chem 38:14–515

    Article  Google Scholar 

  • Molina-Grima E, Sánchez-Pérez JAM, García-Camacho F, Acién-Fernández FG, López-Alonso D, Segura del Castillo CI (1994) Preservation of the marine microalga, Isochrysis galbana: influence of the fatty acid profile. Aquaculture 123:377–385

    Article  CAS  Google Scholar 

  • Muller-Feuga A, Moal J, Kaas R (2007) The microalgae of aquaculture. In: Stφttrup JG, McEvoy LA (eds) Live feeds in marine aquaculture. Blackwell Science, Oxford, pp 207–252

    Google Scholar 

  • Natra FMI, Yusoff FM, Shariff M, Abas F, Mariana NS (2007) Screening of Malaysian indigenous microalgae for antioxidant properties and nutritional value. J Appl Phycol 19:711–718

    Article  Google Scholar 

  • Naviner M, Bergé JP, Durand P, Le Bris H (1999a) Antibacterial activity of the marine diatom Skeletonema costatum against aquacultural pathogens. Aquaculture 174:15–24

    Article  CAS  Google Scholar 

  • Naviner M, Bergé JP, Durand P, Le Bris H (1999b) Vibriostatic bacteria isolated from rearing seawater of oyster brood stock: potentially as biocontrol agent for vibriosis in oyster larvae. Fish Pathol 34:139–144

    Article  Google Scholar 

  • Nobmann P, Bourke P, Dunne J, Henehan G (2010) In vitro antimicrobial activity and mechanism of action of novel carbohydrate fatty acid derivatives against Staphylococcus aureus and MRSA. J Appl Microbiol 108:2152–2161

    CAS  PubMed  Google Scholar 

  • Oppenheimer CH, ZoBell CE (1952) The growth and viability of sixty-three species of marine bacteria as influenced by hydrostatic pressure. J Mar Res 11:10–18

    Google Scholar 

  • Pesando D (1990) Antibacterial and antifungal activities of marine algae. In: Akatsuka I (ed) Introduction to applied phycology. SPB Academic Publishing, The Hague, pp 3–26

    Google Scholar 

  • Phatarpekar PV, Sreepada RA, Pednekar C, Achuthankutty CT (2000) A comparative study on growth performance and biochemical composition of mixed culture of Isochrysis galbana and Chaetoceros calcitrans with monocultures. Aquaculture 181:141–155

    Article  CAS  Google Scholar 

  • Přibyl P, Cepák V, Zachleder V (2013) Production of lipids and formation and mobilization of lipid bodies in Chlorella vulgaris. J Appl Phycol 25:545–553

    Article  Google Scholar 

  • Regunathan C, Wesley SG (2004) Control of Vibrio spp. in shrimp hatcheries using the green algae Tetraselmis suecica. Asian Fish Sci 17:147–158

    Google Scholar 

  • Rico-Mora R, Voltolina D, Villaescusa-Celaya JA (1998) Biological control of Vibrio alginolyticus in Skeletonema costatum (Bacillariophyceae) cultures. Aquac Eng 19:1–6

    Article  Google Scholar 

  • Riquelme CE, Avendaño-Herrera RE (2003) Interacción bacteria–microalga en el ambiente marino y su uso potencial en acuicultura. Rev Chil Hist Nat 76:725–736

    Article  Google Scholar 

  • Riquelme CE, Fukami K, Ishida Y (1988) Effect of bacteria on the growth of a marine diatom, Asterionella gracilis. Bull Jpn Soc Microbiol Ecol 3:29–34

    Article  Google Scholar 

  • Salvesen I, Reitan KI, Skjermo J, Øie G (2000) Microbial environments and marine larviculture: impacts of algal growth rates on the bacterial load in six microalgae. Aquac Int 8:275–287

    Article  Google Scholar 

  • Sánchez-Saavedra MP, Licea-Navarro A, Bernáldez-Sarabia J (2010) Evaluation of the antibacterial activity of different species of phytoplankton. Rev Biol Mar Oceanogr 45:531–536

    Article  Google Scholar 

  • Shamsudin LA (1992) Lipid and fatty acid composition of microalgae used in Malaysian aquaculture as live food for the early stage of penaeid larvae. J Appl Phycol 4:371–378

    Article  CAS  Google Scholar 

  • Shin SY, Bajpai VK, Kim HK, Kang SC (2007) Antibacterial activity of bioconvertes eicosapentanoic (EPA) and docosahexaenoic acid (DHA) against foodborne pathogenic bacteria. Int J Food Microbiol 113:233–236

    Article  CAS  PubMed  Google Scholar 

  • Soffientino B, Gwaltney T, Nelson DR, Specker JL, Mauel M, Gómez-Chiarri M (1999) Infectious necrotizing enteritis and mortality caused by V. carchariae in summer flounder Paralichthys dentatus during intensive cultures. Dis Aquat Org 38:201–210

    Article  CAS  PubMed  Google Scholar 

  • Soto-Rodríguez SA, Roque A, Lizárraga-Partida ML, Guerra-Flores AL, Gómez-Gil B (2003) Virulence of luminous vibrios to Artemia franciscana nauplii. Dis Aquat Org 53:231–240

    Article  PubMed  Google Scholar 

  • Srinivasakumar KP, Rajashekhar M (2009) In vitro studies on bactericidal activity and sensitivity pattern of isolated marine microalgae against selective human bacterial pathogens. Indian J Sci Technol 2:16–23

    CAS  Google Scholar 

  • Tendencia EA, de la Peña M (2003) Investigation of some components of the green water system which makes it effective in the initial control of luminous bacteria. Aquaculture 218:115–119

    Article  Google Scholar 

  • Thompson BA, Swings J (2006) The biology of vibrios. AMS Press, American Society of Microbiology, Washington, DC, p 365

    Google Scholar 

  • Tzovenis I, de Pauw N, Sorgeloos P (1997) Effect of different light regimes on the docosahexaenoic acid (DHA) content of Isochrysis aff. galbana (clone T-ISO). Aquac Intern 5:489–507

    Article  Google Scholar 

  • Wikfors GH, Patterson GW (1994) Differences in strains of Isochrysis of importance to mariculture. Aquaculture 123:127–135

    Article  Google Scholar 

  • Yue X, Liu B, Sun L (2011) Isolation and characterizatiom of virulent Vibrio sp. bacterium from clams (Meretrix meretrix) with mass mortality. J Invertebr Pathol 106:242–249

    Article  CAS  PubMed  Google Scholar 

  • Zhu CJ, Lee YK, Chao TM (1997) Effects of temperature and growth phase on lipid and biochemical composition of Isochrysis galbana TK1. J Appl Phycol 9:451–457

    Article  CAS  Google Scholar 

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Acknowledgement

This work was supported by Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE, Projects 623108 and 682110), Consejo Nacional de Ciencia y Tecnología de México (CONACyT, Project SEP-CONACyT 2009-01-130074), and Fondo Sectorial Salud (Project: 2009-01-114024). We thank L. Trujillo-Valle for technical assistance with the inocula algae production. Guadalupe Vargas Cárdenas, curator of the CICESE collection of microorganisms, provided us with the reference strains.

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  1. Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Carretera Tijuana-Ensenada 3918, Zona Playitas, 22860, Ensenada, Baja California, México

    Ceres A. Molina-Cárdenas, M. del Pilar Sánchez-Saavedra & Marcial L. Lizárraga-Partida

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  1. Ceres A. Molina-Cárdenas
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  2. M. del Pilar Sánchez-Saavedra
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Molina-Cárdenas, C.A., Sánchez-Saavedra, M.d.P. & Lizárraga-Partida, M.L. Inhibition of pathogenic Vibrio by the microalgae Isochrysis galbana . J Appl Phycol 26, 2347–2355 (2014). https://doi.org/10.1007/s10811-014-0270-1

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