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Preliminary study on the response of marine fungoid protists, the thraustochytrids, to lipid extracts of diatoms

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Abstract

Thraustochytrids are particle-associated protists, ubiquitous in the marine environment. They are known to display a negative relationship with phytoplankton cells but a positive one with their exudates and detritus. Phytoplankton are known to express allelopathic effects against other organisms, but the exact mechanism by which phytoplankton cause inhibition to thraustochytrids is understudied. This is the first report of examination of bioactivity of lipid extracts of diatom cultures on thraustochytrids. Lipid extracts from four diatom cultures, viz. Cylindrotheca closterium (JB2), Skeletonema sp.1 (JB3), Thalassiosira sp. (JB4) and Skeletonema sp.2 (JB5), were tested against the growth of thraustochytrids: Oblongichytrium spp. (isolates VD4 and VD6), Parietichytrium sp. (isolate VD12) and Schizochytrium sp. (isolate VDC23b). Among the thraustochytrid isolates, Parietichytrium sp. was the most sensitive, whereas Schizochytrium sp. appeared to be the most resistant to the lipid extracts. The lipid extract from C. closterium possessed high amounts of C16:0, C16:1, C18:0, C18:1 and C20:5 fatty acids and bioactivity against the thraustochytrids. Lipids extracted during the late stationary phase of diatoms were inhibitory to thraustochytrid growth. Overall, these observations not only enhance our understanding of the diversity of allelopathic interactions between thraustochytrids and diatoms in the marine ecosystem, but also reveal the pivotal role of diatom lipids in such interactions across trophic levels.

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References

  • Amin SA, Parker MS, Armbrust EV (2012) Interactions between diatoms and bacteria. Microbiol Mol Biol Rev 76:667–684

    CAS  PubMed  PubMed Central  Google Scholar 

  • Armbrecht LH, Smetacek V, Assmy P, Klaas C (2014) Cell death and aggregate formation in the giant diatom Coscinodiscus wailesii (Gran & Angst, 1931). J Exp Mar Biol Ecol 452:31–39

    Google Scholar 

  • Azam F, Long RA (2001) Sea snow microcosms. Nature 414:495–498

    CAS  PubMed  Google Scholar 

  • Berdjeb L, Parada A, Needham DM, Fuhrman JA (2018) Short-term dynamics and interactions of marine protist communities during the spring-summer transition. ISME J 12:1907–1917

    PubMed  PubMed Central  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Phys 37:911–917

    CAS  Google Scholar 

  • Bochdansky AB, Clouse MA, Herndl GJ (2017) Eukaryotic microbes, principally fungi and labyrinthulomycetes, dominate biomass on bathypelagic marine snow. ISME J 11:362–373

    PubMed  Google Scholar 

  • Daly KL, Passow U, Chanton J, Hollander D (2016) Assessing the impacts of oil-associated marine snow formation and sedimentation during and after the Deepwater Horizon oil spill. Anthropocene 13:18–33

    Google Scholar 

  • Damare VS (2019) Chapter 30. Advances in isolation and preservation strategies of ecologically important marine protists, the thraustochytrids. In: Meena SN, Naik MM (eds) Advances in biological science research. Elsevier, Amsterdam, pp 485–500

    Google Scholar 

  • Damare V, Raghukumar S (2006) Morphology and physiology of the marine straminipilan fungi, the aplanochytrids isolated from the equatorial Indian Ocean. Indian J Mar Sci Spec Issue Mar Mycol 35:326–340

    Google Scholar 

  • Damare V, Raghukumar S (2008) Abundance of thraustochytrids and bacteria in the equatorial Indian Ocean, in relation to Transparent Exopolymeric Particles (TEPs). FEMS Microbiol Ecol 65:40–49

    CAS  PubMed  Google Scholar 

  • Damare VS, Raghukumar S (2010) Association of the stramenopilan protists, the aplanochytrids, with zooplankton of the equatorial Indian Ocean. Mar Ecol Prog Ser 399:53–68

    CAS  Google Scholar 

  • Damare VS, Raghukumar S (2012) Marine aggregates and transparent exopolymeric particles (TEPs) as substrates for the stramenopilan fungi, the thraustochytrids: roller table experimental approach. Kavaka 40:22–31

    Google Scholar 

  • Damare VS, Raghukumar S (2015) Apparent grazing losses of Labyrinthulomycetes protists in oceanic and coastal waters: an experimental elucidation. Ecol Res 30:403–414

    Google Scholar 

  • Damare VS, Damare S, Ramanujam P, Meena RM (2013) Preliminary studies on the association between zooplankton and the stramenopilan fungi, aplanochytrids. Microbial Ecol 65:955–963

    CAS  Google Scholar 

  • Decho AW, Gutierrez T (2017) Microbial extracellular polymeric substances (EPSs) in ocean systems. Frontiers Microbiol 8:922. https://doi.org/10.3389/fmicb.2017.00922

    Article  Google Scholar 

  • Demirel Z, Imamoglu E, Dalay MC (2015) Fatty acid profile and lipid content of Cylindrotheca closterium cultivated in air-lift photobioreactor. J Chem Technol Biotechnol 90:2290–2296

    CAS  Google Scholar 

  • Duan Y, Sen B, Xie N, Paterson JS, Chen Z, Wang G (2018) Flow cytometry for rapid enumeration and biomass quntification of thraustochytrids in coastal seawaters. Microbes Environ 33:195–204

    PubMed  PubMed Central  Google Scholar 

  • Fay JP, Farias RN (1975) The inhibitory action of fatty acids on the growth of Escherichia coli. J Gen Microbiol 91:233–240

    CAS  PubMed  Google Scholar 

  • Gaertner A (1979) Some fungal parasites found in the diatom populations of the Rusfjord area (South Norway) during March 1979. Veröff Inst Meeresforsch Bremerh 18:29–33

    Google Scholar 

  • Georges C, Monchy S, Genitsaris S, Christaki U (2014) Protist community composition during early phytoplankton blooms in the naturally iron-fertilized Kerguelen area (Southern Ocean). Biogeosciences 11:5847–5863

    Google Scholar 

  • Guihéneuf F, Mimouni V, Ulmann L, Tremblin G (2008) Environmental factors affecting growth and omega 3 fatty acid composition in Skeletonema costatum. The influences of irradiance and carbon source. Diatom Res 23:93–103

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Hamamoto Y, Honda D (2019) Nutritional intake of Aplanochytrium (Labyrinthule, Stramenopiles) from living diatoms revealed by culture experiments suggesting the new prey-predator interactions in the grazing food web of the marine ecosystem. PLoS ONE 14:e0208941

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Q, Sommerfeld M, Jarvis E, Ghirardi M (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54:621–639

    CAS  PubMed  Google Scholar 

  • Huang CB, Altimova Y, Myers TM, Ebersole JL (2011) Short- and medium-chain fatty acids exhibit antimicrobial activity for oral microorganisms. Arch Oral Biol 56:650–654

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jain R, Raghukumar S, Tharanathan R, Bhosle NB (2005) Extracellular polysaccharide production by thraustochytrid protists. Mar Biotechnol 7:184–192

    CAS  Google Scholar 

  • Kimura H, Sato M, Sugiyama C, Naganuma T (2001) Coupling of thraustochytrids and POM, and of bacterio- and phytoplankton in a semi-enclosed coastal area: implication for different substrate preference by the planktonic decomposers. Aquat Microb Ecol 25:293–300

    Google Scholar 

  • Leaño EM, Damare VS (2012) Chapter 12. Labyrinthulomycota. In: Jones EBG, Pang K-L (eds) Marine fungi and fungal-like organisms. Walter de Gruyter GmbH, Berlin, pp 215–243

    Google Scholar 

  • Li Q, Wang X, Liu X, Jiao N (2013) Abundance and novel lineages of thraustochytrids in Hawaiian waters. Microbial Ecol 66:823–830

    Google Scholar 

  • Liu Y, Singh P, Sun Y, Luan S, Wang G (2014) Culturable diversity and biochemical features of thraustochytrids from coastal waters of Southern China. Appl Microbiol Biotechnol 98:3241–3255

    CAS  PubMed  Google Scholar 

  • López-García P, Rodriguez-Valera F, Pedrós-Alió C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603–607

    PubMed  Google Scholar 

  • Lyons MM, Ward JE, Smolowitz R, Uhlinger KR (2005) Lethal marine snow: pathogen of bivalve mollusc concealed in marine aggregates. Limnol Oceanogr 50:1983–1988

    Google Scholar 

  • Mamatha SS, Halami PM, Venkateswaran G (2010) Identification and characterization of the n-6 fatty acid-producing Mucor rouxii native isolate CFR-G15. Eur J Lipid Sci Technol 112:380–389

    CAS  Google Scholar 

  • Marchan LF, Chang KJL, Nichols PD, Mitchell WJ, Polglase JL, Gutierrez T (2018) Taxonomy, ecology and biotechnological applications of thraustochytrids: a review. Biotechnol Adv 36:26–46

    Google Scholar 

  • Naganuma T, Takasugi H, Kimura H (1998) Abundance of thraustochytrids in coastal plankton. Mar Ecol Prog Ser 162:105–110

    Google Scholar 

  • Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological seawater analysis. Pergamon, New York

    Google Scholar 

  • Prartono T, Kawaroe M, Katii V (2013) Fatty acid composition of three diatom species Skeletonema costatum, Thalassiosira sp. and Chaetoceros gracilis. Int J Environ Bioenergy 6:28–43

    CAS  Google Scholar 

  • Pratoomyot J, Srivilas P, Noiraksar T (2005) Fatty acids composition of 10 microalgal species. Songklanakarin J Sci Technol 27:1179–1187

    Google Scholar 

  • Raghukumar C (1986) Fungal parasites of the marine green algae, Cladophora and Rhizoclonium. Bot Mar 29:289–297

    Google Scholar 

  • Raghukumar S (2002) Ecology of the marine protists, the Labyrinthulomycetes (Thraustochytrids and Labyrinthulids). Eur J Protistol 38:127–145

    Google Scholar 

  • Raghukumar S (2008) Thraustochytrid marine protists: production of PUFAs and other emerging technologies. Mar Biotechnol 10:631–640

    CAS  Google Scholar 

  • Raghukumar S (2017) Chapter 11. The pelagic ecosystem. In: Raghukumar S (ed) Fungi in coastal and oceanic marine ecosystems. Springer, Berlin, pp 173–205

    Google Scholar 

  • Raghukumar S, Damare VS (2011) Increasing evidence for the important role of Labyrinthulomycetes in marine ecosystems. Bot Mar 54:3–11

    Google Scholar 

  • Raghukumar C, Nagarkar S, Raghukumar S (1992) Association of thraustochytrids and fungi with living marine algae. Mycol Res 96:542–546

    Google Scholar 

  • Raghukumar S, Anil AC, Khandeparker L, Patil JS (2000) Thraustochytrid protists as a component of marine microbial films. Mar Biol 136:603–609

    Google Scholar 

  • Raghukumar S, Ramaiah N, Raghukumar C (2001) Dynamics of thraustochytrid protists in the water column of the Arabian Sea. Aquat Microb Ecol 24:175–186

    Google Scholar 

  • Raikar MT, Raghukumar S, Vani V, David JJ, Chandramohan D (2001) Thraustochytrid protists degrade hydrocarbons. Indian J Mar Sci 30:139–145

    CAS  Google Scholar 

  • Rapp JZ, Fernández-Méndez M, Bienhold C, Boetius A (2018) Effects of ice-algal aggregate export on the connectivity of bacterial communities in the Central Arctic Ocean. Front Microbiol 9:1035. https://doi.org/10.3389/fmicb.2018.01035

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodríguez-Núñez K, Toledo-Agüero P (2017) Fatty acids profile and nutritional composition of two tropical diatoms from the Costa Rican Pacific Coast. Grasas Aceites 68:e209. https://doi.org/10.3989/gya.1276162

    Article  CAS  Google Scholar 

  • Scholz B, Guillou L, Marano AV, Neuhauser S, Sullivan BK, Karsten U, Küpper FC, Gleason FH (2016) Zoosporic parasites infecting marine diatoms—a black box that needs to be opened. Fungal Ecol 19:59–76

    PubMed  PubMed Central  Google Scholar 

  • Suroy M, Moriceau B, Boutorh J, Goutx M (2014) Fatty acids associated with the frustules of diatoms and their fate during degradation—a case study in Thalassiosira weissflogii. Deep Sea Res Pt I 86:21–31

    CAS  Google Scholar 

  • Ueda M, Nomura Y, Doi K, Nakajima M (2015) Seasonal dynamics of culturable thraustochytrids (Labyrinthulomycetes, Stramenopiles) in estuarine and coastal waters. Aquat Microb Ecol 74:187–204

    Google Scholar 

  • Volkman JK, Hallegraeff GM (1988) Lipids in marine diatoms of the genus Thalassiosira: predominance of 24-methylenecholesterol. Phytochemistry 27:1389–1394

    CAS  Google Scholar 

  • White TJ, Bruns TD, Lee SB, Taylor JW (1990) Analysis of phylogenetic relationships by amplification and direct sequencing of ribosomal DNA genes. In: Innis DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322

    Google Scholar 

  • Xu N, Tang YZ, Qin J, Duan S, Gobler CJ (2015) Ability of the marine diatoms Pseudo-nitzschia multiseries and P. pungens to inhibit the growth of co-occurring phytoplankton via allelopathy. Aquat Microb Ecol 74:29–41

    Google Scholar 

  • Yi Z, Xu M, Di X, Brynjolfsson S (2017) Exploring valuable lipids in diatoms. Front Mar Sci 4:17. https://doi.org/10.3389/fmars.2017.00017

    Article  Google Scholar 

  • Yokoyama R, Salleh B, Honda D (2007) Taxonomic rearrangement of the genus Ulkenia sensu lato based on morphology, chemotaxonomical characteristics, and 18S rRNA gene phylogeny (thraustochytriaceae, Labyrinthulomycetes): emendation for Ulkenia and erection of Botryochytrium, Parietichytrium, and Sicyoidochytrium gen. nov. Mycoscience 48:329–341

    CAS  Google Scholar 

  • Zhukova NV (2004) Changes in the lipid composition of Thalassiosira pseudonana during its life cycle. Russ J Plant Physiol 51:702–707

    CAS  Google Scholar 

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Acknowledgements

Authors are extremely grateful to Dr. Samir Damare, Senior Scientist, CSIR-National Institute of Oceanography (CSIR-NIO) and the Director of the same institute for allowing to use their laboratory facility to carry out the molecular work. Help rendered by Mr. Ram Murti Meena, CSIR-NIO, for sequencing is highly acknowledged. Authors would also like to thank the Head of the Department of Microbiology, Goa University, for providing basic facilities for growth and maintenance of thraustochytrid and diatom cultures. Authors are extremely thankful to Ms. Judith Noronha-Carvalho for providing the diatom cultures for this work and to Ms. Fazila Shaikh for assistance in bulk culturing of the diatoms for lipid analysis. PD would like to acknowledge the Science and Engineering Research Board, Department of Science and Technology, Government of India, for the SERB-DST Fast Track Project for Young Scientists (DST No: SB/YS/LS-319/2013).

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Damare, V.S., D’Costa, P.M., Shivaramu, M.S. et al. Preliminary study on the response of marine fungoid protists, the thraustochytrids, to lipid extracts of diatoms. Aquat Ecol 54, 355–367 (2020). https://doi.org/10.1007/s10452-020-09747-z

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