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Diversity of thraustochytrid protists isolated from brown alga, Sargassum cinereum using 18S rDNA sequencing and their morphological response to heavy metals

Published online by Cambridge University Press:  11 November 2014

Varada S. Damare
Varada S. Damare*
Affiliation:
Biological Oceanography Division, CSIR-National Institute of Oceanography, Dona Paula, Goa 403004, India
*
Correspondence should be addressed to: V.S. Damare, Biological Oceanography Division, CSIR-National Institute of Oceanography, Dona Paula, Goa 403004, India email: vdamare@nio.org, chimulkarvarada@gmail.com
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Abstract

Thraustochytrids, the exclusively marine organisms of kingdom Stramenopila and a source of essential fatty acids in the marine milieu, possess an osmoheterotrophic mode of nutrition and are therefore affected by type and source of available organic matter and pollution. To study their response to heavy metal pollution, they were isolated from the brown alga Sargassum cinereum from the coastal waters of Dona Paula, Goa, India. A total of 22 isolates were obtained from two samples collected during February and March 2012. Based on their 18S rRNA gene sequencing, the majority of the isolates were identified as Thraustochytrium kinnei. The rest were identified to be Sicyoidochytrium minutum, Ulkenia visurgensis and species of Thraustochytrium and Aurantiochytrium. Six isolates were screened for various enzymatic activities. Characteristic and distinctive enzyme profile was obtained from isolates of different genera. All isolates were also screened for their tolerance to heavy metals. They showed good growth in the presence of Mn2+. The other metals that were tolerated by most of the isolates were in the order Ni2+ > Cr6+ > Zn2+. Seven isolates grew in the presence of Cu2+, and six in the presence of Cd2+. The isolates growing on metals showed vast differences from their normal morphology such as small colony size, shrunken cells etc. Scanning electron micrographs revealed holes or depressions in the cell wall in the presence of metals. On the whole, the isolates belonging to Ulkenia visurgensis and Aurantiochytrium sp. showed tolerance to more metals than Thraustochytrium kinnei. Cluster analysis showed no peculiar trend of metal tolerance to any particular genus as the characters were scattered in the clusters.

Keywords

thraustochytridsmarineLabyrinthulomycotaStramenopilaSargassumbrown algaheavy metals
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 95 , Issue 2 , March 2015 , pp. 265 - 276
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

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References

Antunes, W.M., Luna, A.S., Henriques, C.A. and da Costa, A.C.A. (2003) An evaluation of copper biosorption by a brown seaweed under optimized conditions. Electronic Journal of Biotechnology 6, 174–180.Google Scholar
Armstrong, E., Yan, L., Boyd, K.G., Wright, P.C. and Burgess, J.G. (2001) The symbiotic role of marine microbes on living surfaces. Hydrobiologia 461, 37–40.CrossRefGoogle Scholar
Badrinathan, S., Shiju, T.M., Sharon, C.A.S., Arya, R. and Pragasam, V. (2012) Purification and structural characterization of sulfated polysaccharide from Sargassum myriocystum and its efficacy in scavenging free radicals. Indian Journal of Pharmaceutical Sciences 74, 549–555.Google ScholarPubMed
Bazes, A., Silkina, A., Douzene, P., Faÿ, F., Kervarec, N., Morin, D., Berge, J-P. and Bourgougnon, N. (2009) Investigation of the antifouling constituents from the brown alga Sargassum muticum (Yendo) Fensholt. Journal of Applied Phycology 21, 395–403.CrossRefGoogle Scholar
Bongiorni, L., Pusceddu, A. and Danovaro, R. (2005) Enzymatic activities of epiphytic and benthic thraustochytrids involved in organic matter degradation. Aquatic Microbial Ecology 41, 299–305.CrossRefGoogle Scholar
Bourne, P.C., Isupov, M.N. and Littlechild, J.A. (2000) The atomic-resolution structure of a novel bacterial esterase. Structure 8, 143–151.CrossRefGoogle ScholarPubMed
Chamberlain, A.H.L. (1980) Cytochemical and ultrastructural studies on the cell walls of Thraustochytrium spp. Botanica Marina 23, 669–677.CrossRefGoogle Scholar
Coston-Clements, L., Settle, L.R., Hoss, D.E. and Cross, F.A. (1991) Utilization of the Sargassum habitat by marine invertebrates and vertebrates – a review. NOAA Technical Memorandum NMFS-SEFSC-296, 32 pp.Google Scholar
Culotta, V.C., Yang, M. and Hall, M.D. (2005) Manganese transport and trafficking: lessons learned from Saccharomyces cerevisiae. Eukaryotic Cell 4, 1159–1165.CrossRefGoogle ScholarPubMed
Damare, V. and Raghukumar, S. (2008) Abundance of thraustochytrids and bacteria in the equatorial Indian Ocean, in relation to Transparent Exopolymeric Particles (TEPs). FEMS Microbiology Ecology 65, 40–49.CrossRefGoogle ScholarPubMed
Damare, V. and Raghukumar, S. (2010) Association of the stramenopilan protists, the aplanochytrids, with zooplankton of the equatorial Indian Ocean. Marine Ecology Progress Series 399, 53–68.CrossRefGoogle Scholar
Damare, V.S., Damare, S., Ramanujam, P., Meena, R.M. and Raghukumar, S. (2013) Preliminary studies on the association between zooplankton and the Stramenopilan fungi, aplanochytrids. Microbial Ecology 65, 955–963.CrossRefGoogle ScholarPubMed
Das, N., Vimala, R. and Karthika, P. (2008) Biosorption of heavy metals – an overview. Indian Journal of Biotechnology 7, 159–169.Google Scholar
Dinu, L-D., Anghel, L. and Jurcoane, S. (2011) Isolation of heavy metal resistant bacterial strains from the battery manufactured polluted environment. Romanian Biotechnological Letters 16, 102–106.Google Scholar
Dodgson, K.S., Lewis, J.I.M. and Spencer, B. (1953) Studies on sulphatases 3. The arylsulphatase and β-glucuronidase of marine mollusks. Biochemical Journal 55, 253–259.CrossRefGoogle Scholar
Harel, M., Ben- Dov, E., Rasoulouniriana, D., Siboni, N., Kramarsky-Winter, E., Loya, Y., Barak, Z., Wiesman, Z. and Kushmaro, A. (2008) A new thraustochytrid, strain Fng1, isolated from the surface mucus of the hermatypic coral Fungia granulose. FEMS Microbiology Ecology 64, 378–387.CrossRefGoogle Scholar
Hollants, J., Leliaert, F., De Clerck, O. and Willems, A. (2013) What we can learn from sushi: a review on seaweed-bacterial associations. FEMS Microbiology Ecology 83, 1–16.CrossRefGoogle ScholarPubMed
Honda, D., Yokochi, T., Nakahara, T., Raghukumar, S., Nakagiri, A., Schaumann, K. and Higashihara, T. (1999) Molecular phylogeny of labyrinthulids and thraustochytrids based on the sequencing of 18S ribosomal RNA gene. Journal of Eukaryotic Microbiology 46, 637–647.CrossRefGoogle ScholarPubMed
Jain, R., Raghukumar, S., Tharanathan, R. and Bhosle, N.B. (2005) Extracellular polysaccharide production by thraustochytrid protists. Marine Biotechnology 7, 184–192.CrossRefGoogle ScholarPubMed
Kalab, M., Yang, A.-F. and Denise, C. (2008) Conventional scanning electron microscopy of bacteria. Infocus Magazine 10, 42–61.CrossRefGoogle Scholar
Krishnakumar, P.K., Pillai, V.K. and Valsala, K.K. (1990) Bioaccumulation of trace metals by marine flora and fauna near a caustic soda plant (Karwar, India). Indian Journal of Fisheries 37, 129–137.Google Scholar
Kuenzler, E.J. and Perras, J.P. (1965) Phosphatases of marine algae. Biological Bulletin 128, 271–284.CrossRefGoogle Scholar
Lin, Y.C., Leaño, E.M. and Pang, K.L. (2010) Effects of Cu(II) and Zn(II) on growth and cell morphology of thraustochytrids isolated from fallen mangrove leaves in Taiwan. Botanica Marina 53, 581–586.CrossRefGoogle Scholar
Miersch, J., Bärlocher, F., Bruns, I. and Krauss, G-J. (1997) Effects of cadmium, copper, and zinc on growth and thiol content of aquatic hyphomycetes. Hydrobiologia 346, 77–84.CrossRefGoogle Scholar
Miller, J.D. and Jones, E.B.G. (1983) Observations on the association of thraustochytrid marine fungi with decaying seaweed. Botanica Marina 26, 345–351.CrossRefGoogle Scholar
Penesyan, A., Marshall-Jones, Z., Holmstrom, C., Kjelleberg, S. and Egan, S. (2009) Antimicrobial activity observed among cultured marine epiphytic bacteria reflects their potential as a source of new drugs. FEMS Microbiology Ecology 69, 113–124.CrossRefGoogle ScholarPubMed
Poli, A., Anzelmo, G. and Nicolaus, B. (2010) Bacterial exopolysacchardies from extreme marine habitats: production, characterization and biological activities. Marine Drugs 8, 1779–1802.CrossRefGoogle ScholarPubMed
Porter, D. and Lingle, W.L. (1992) Endolithic thraustochytrid marine fungi from planted shell fragments. Mycologia 84, 289–299.CrossRefGoogle Scholar
Raghukumar, C., Mohandass, C., Cardigos, F., D'Costa, P.M., Santos, R.S. and Colaço, A. (2008) Assemblage of benthic diatoms and culturable heterotrophs in shallow-water hydrothermal vent of D. João de Castro Seamount, Azores in the Atlantic Ocean. Current Science 95, 1715–1723.Google Scholar
Raghukumar, S. (1988) Schizochytrium mangrovei sp. nov., a thraustochytrid from mangroves in India. Transactions of the British Mycological Society 90, 627–631.CrossRefGoogle Scholar
Raghukumar, S. (2002) Ecology of the marine protists, the Labyrinthulomycetes (Thraustochytrids and Labyrinthulids). European Journal of Protistology 38, 127–145.CrossRefGoogle Scholar
Raghukumar, S. (2008) Thraustochytrid marine protists: production of PUFAs and other emerging technologies. Marine Biotechnology 10, 631–640.CrossRefGoogle ScholarPubMed
Raghukumar, S. and Damare, V. S. (2011) Increasing evidence for the important role of Labyrinthulomycetes in marine ecosystems. Botanica Marina 54, 3–11.CrossRefGoogle Scholar
Sathe-Pathak, V., Raghukumar, S., Raghukumar, C. and Sharma, S. (1993) Thraustochytrid and fungal component of marine detritus. I. Field studies on decomposition of the brown alga Sargassum cinereum J. Ag. Indian Journal of Marine Sciences 22, 159–167.Google Scholar
Sharma, S., Raghukumar, C., Raghukumar, S., Sathe-Pathak, V. and Chandramohan, D. (1994) Thraustochytrid and fungal component of marine detritus II. Laboratory studies on decomposition of the brown alga Sargassum cinereum. J. Ag. Journal of Experimental Marine Biology and Ecology 175, 227–242.CrossRefGoogle Scholar
Singh, P., Raghukumar, C., Parvatkar, R.R. and Mascarenhas-Pereira, M.B.L. (2013) Heavy metal tolerance in the psychrotolerant Cryptococcus sp. isolated from deep-sea sediments of the Central Indian Basin. Yeast 30, 93–101.CrossRefGoogle ScholarPubMed
Soria-Mercado, I.E., Villarreal-Gómez, L.J., Rivas, G.G. and Sánchez, N.E.A. (2012) Bioactive compounds from bacteria associated to marine algae. In Sammour, R.H. (ed.) Biotechnology – molecular studies and novel applications for improved quality of human life. InTech Europe, pp. 25–43.Google Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.CrossRefGoogle ScholarPubMed
Turner, J.P. and Rooker, J.R. (2006) Fatty acid composition of flora and fauna associated with Sargassum mats in the Gulf of Mexico. Marine Biology 149, 1025–1036.CrossRefGoogle Scholar
Volesky, B. and Holan, Z. R. (1995) Biosorption of heavy metals. Biotechnology Progress 11, 235–250.CrossRefGoogle ScholarPubMed
Wagner-Döbler, I., Beil, W., Lang, S., Meiners, M. and Laatsch, H. (2002) Integrated approach to explore the potential of marine microorganisms for the production of bioactive metabolites. Advances in Biochemical Engineering/Biotechnology 74, 207–238.CrossRefGoogle ScholarPubMed
Weete, J.D., Kim, H., Gandhi, S.R., Wang, Y. and Dute, R. (1997) Lipids and ultrastructure of Thraustochytrium sp. ATCC 26185. Lipids 32, 839–845.CrossRefGoogle ScholarPubMed
White, T.J., Bruns, T.D., Lee, S.B. and Taylor, J.W. (1990) Analysis of phylogenetic relationships by amplification and direct sequencing of ribosomal DNA genes. In Innis, D.H., Sninsky, J.J. and White, T.J. (eds) PCR protocols: a guide to methods and applications. New York: Academic Press, pp. 315–322.Google Scholar
Yang, J. and Volesky, B. (1999) Biosorption of uranium on Sargassum biomass. Water Research 33, 3357–3363.CrossRefGoogle Scholar
Yokoyama, R. and Honda, D. (2007) Taxonomic rearrangement of the genus Schizochytrium sensu lato based on morphology, chemotaxonomical characteristics, and 18S rRNA gene phylogeny (Thraustochytriaceae, Labyrinthulomycetes): emendation for Schizochytrium and erection of Aurantiochytrium and Oblongichytrium gen. nov. Mycoscience 48, 199–211.CrossRefGoogle Scholar
Yu, C., Lee, A.M., Bassler, B.L. and Roseman, S. (1991) Chitin utilization by marine bacteria. A physiological function for bacterial adhesion to immobilized carbohydrates. Journal of Biological Chemistry 266, 24260–24267.CrossRefGoogle ScholarPubMed