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Prospective enzymes for omega-3 PUFA biosynthesis found in endoparasitic classes within the phylum Platyhelminthes

Published online by Cambridge University Press:  10 December 2020

D. Babaran ,
M.T. Arts ,
R.J. Botelho ,
S.A. Locke  and
J. Koprivnikar Open the ORCID record for J. Koprivnikar [Opens in a new window]
D. Babaran
Affiliation:
Department of Chemistry and Biology, Ryerson University, Toronto, Ontario, Canada
M.T. Arts
Affiliation:
Department of Chemistry and Biology, Ryerson University, Toronto, Ontario, Canada
R.J. Botelho
Affiliation:
Department of Chemistry and Biology, Ryerson University, Toronto, Ontario, Canada
S.A. Locke
Affiliation:
Department of Biology, University of Puerto Rico, Mayagüez, Puerto Rico, USA
J. Koprivnikar*
Affiliation:
Department of Chemistry and Biology, Ryerson University, Toronto, Ontario, Canada
*
Author for correspondence: J. Koprivnikar, E-mail: jkoprivn@ryerson.ca
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Abstract

The free-living infectious stages of macroparasites, specifically, the cercariae of trematodes (flatworms), are likely to be significant (albeit underappreciated) vectors of nutritionally important polyunsaturated fatty acids (PUFA) to consumers within aquatic food webs, and other macroparasites could serve similar roles. In the context of de novo omega-3 (n-3) PUFA biosynthesis, it was thought that most animals lack the fatty acid (FA) desaturase enzymes that convert stearic acid (18:0) into ɑ-linolenic acid (ALA; 18:3n-3), the main FA precursor for n-3 long-chain PUFA. Recently, novel sequences of these enzymes were recovered from 80 species from six invertebrate phyla, with experimental confirmation of gene function in five phyla. Given this wide distribution, and the unusual attributes of flatworm genomes, we conducted an additional search for genes for de novo n-3 PUFA in the phylum Platyhelminthes. Searches with experimentally confirmed sequences from Rotifera recovered nine relevant FA desaturase sequences from eight species in four genera in the two exclusively endoparasite classes (Trematoda and Cestoda). These results could indicate adaptations of these particular parasite species, or may reflect the uneven taxonomic coverage of sequence databases. Although additional genomic data and, particularly, experimental study of gene functionality are important future validation steps, our results indicate endoparasitic platyhelminths may have enzymes for de novo n-3 PUFA biosynthesis, thereby contributing to global PUFA production, but also representing a potential target for clinical antihelmintic applications.

Keywords

platyhelminthomega fatty acidpolyunsaturatedbiosynthesisparasite
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e212
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Altschul, SF, Madden, TL, Schäffer, AA, Zhang, J, Zhang, Z, Miller, W and Lipman, DJ (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.CrossRefGoogle ScholarPubMed
Arakelova, KS, Chebotareva, MA and Zabelinskii, SA (2004) Physiology and lipid metabolism of Littorina saxatilis infected with trematodes. Diseases of Aquatic Organisms 60, 223–231.CrossRefGoogle ScholarPubMed
Arts, MT, Ackman, RG and Holub, BJ (2001) ‘Essential fatty acid’ in aquatic ecosystems: A crucial link between diet and human health and evolution. Canadian Journal of Fisheries and Aquatic Sciences 58, 122–137.CrossRefGoogle Scholar
Assis, R and Kondrashov, AS (2014) Conserved proteins are fragile. Molecular Biology and Evolution 31, 419–424.CrossRefGoogle ScholarPubMed
Belley, A and Chadee, K (1995) Eicosanoid production by parasites: From pathogenesis to immunomodulation? Parasitology Today 11, 327–334.CrossRefGoogle ScholarPubMed
Bernt, M, Bleidorn, C, Braband, A, et al. (2013) A comprehensive analysis of bilaterian mitochondrial genomes and phylogeny. Molecular Phylogenetics and Evolution 69, 352–364.CrossRefGoogle ScholarPubMed
Bexkens, ML, Mebius, MM, Houweling, M, Brouwers, JF, Tielens, AG and van Hellemond, JJ (2019) Schistosoma mansoni does not and cannot oxidise fatty acids, but these are used for biosynthetic purposes instead. International Journal for Parasitology 49, 647–656.CrossRefGoogle Scholar
Brant, SV and Loker, ES (2005) Can specialized pathogens colonize distantly related hosts? Schistosome evolution as a case study. PLoS Pathogens 1, e38.CrossRefGoogle ScholarPubMed
Brett, M and Müller-Navarra, D (1997) The role of highly unsaturated fatty acids in aquatic food web processes. Freshwater Biology 38, 483–499.CrossRefGoogle Scholar
Buckner, J and Hagen, M (2003) Triacylglycerol and phospholipid fatty acids of the silverleaf whitefly: Composition and biosynthesis. Archives of Insect Biochemistry and Physiology 53, 66–79.CrossRefGoogle ScholarPubMed
Castro, LFC, Tocher, DR and Monroig, Ó (2016) Long-chain polyunsaturated fatty acid biosynthesis in chordates: Insights into the evolution of FADS and ELOVL gene repertoire. Progress in Lipid Research 62, 25–40.CrossRefGoogle ScholarPubMed
Chen, B and Wen, JF (2011) The adaptive evolution divergence of triosephosphate isomerases between parasitic and free-living flatworms and the discovery of a potential universal target against flatworm parasites. Parasitology Research 109, 283–289.CrossRefGoogle ScholarPubMed
Clark, K, Karsch-Mizrachi, I, Lipman, DJ, Ostell, J and Sayers, EW (2016) Genbank. Nucleic Acids Research 44, D67–D72.CrossRefGoogle ScholarPubMed
Colombo, SM, Rodgers, TFM, Diamond, ML, Bazinet, RP and Arts, MT (2020) Projected declines in global DHA availability for human consumption as a result of global warming. Ambio 49, 865–880.CrossRefGoogle ScholarPubMed
Das, UN (2006) Essential fatty acids: Biochemistry, physiology and pathology. Biotechnology Journal 1, 420–439.CrossRefGoogle ScholarPubMed
Daugschies, A and Joachim, A (2000) Eicosanoids in parasites and parasitic infections. Advances in Parasitology 46, 182–240.Google ScholarPubMed
Edgecombe, GD, Giribet, G, Dunn, CW, Hejnol, A, Kristensen, RM, Neves, RC, Rouse, GW, Worsaae, K and Sørensen, MV (2011) Higher-level metazoan relationships: Recent progress and remaining questions. Organisms Diversity & Evolution 11, 151–172.CrossRefGoogle Scholar
Egger, B, Lapraz, F, Tomiczek, B, et al. (2015) A transcriptomic-phylogenomic analysis of the evolutionary relationships of flatworms. Current Biology 25, 1347–1353.CrossRefGoogle ScholarPubMed
Esch, GW, Barger, MA and Fellis, KJ (2002) The transmission of digenetic trematodes: Style, elegance, complexity. Integrative and Comparative Biology 42, 304–312.CrossRefGoogle ScholarPubMed
Fellous, S and Salvaudon, L (2008) How can your parasites become your allies? Trends in Parasitology 25, 62–66.CrossRefGoogle Scholar
Ferraz, RB, Kabeya, N, Lopes-Marques, M, Machado, AM, Ribeiro, RA, Salaro, AL, Ozório, R, Castro, LFC and Monroig, Ó (2019) A complete enzymatic capacity for long-chain polyunsaturated fatty acid biosynthesis is present in the Amazonian teleost tambaqui, Colossoma Macropomum. Comparative Biochemistry and Physiology, Part B 227, 90–97.CrossRefGoogle ScholarPubMed
Fried, B and Sherma, J (1990) Thin layer chromatography of lipids found in snails (Gastropoda: Mollusca). Journal of Planar Chromatography 3, 290–299.Google Scholar
Fried, B and Toledo, R (2009) The biology of echinostomes: From the molecule to the community. 333 pp. Springer Science and Business Media. New York.Google Scholar
Furlong, ST (1991) Unique roles for lipids in Schistosoma mansoni. Parasitology Today 7, 59–62.CrossRefGoogle ScholarPubMed
Galaktionov, KV and Skirnisson, K (2007) New data on Microphallus breviatus Deblock & Maillard, 1975 (Microphallidae: Digenea) with emphasis on the evolution of dixenous life cycles of microphallids. Parasitology Research 100, 963–971.CrossRefGoogle ScholarPubMed
Gladyshev, M, Arts, M and Sushchik, N (2009) Preliminary estimates of the export of omega-3 highly unsaturated fatty acids (EPA + DHA) from aquatic to terrestrial ecosystems. pp. 179–209 in Kainz, M, Brett, M, Arts, M (Eds) Lipids in aquatic ecosystems. New York, Springer.CrossRefGoogle ScholarPubMed
Gratraud, P, Huws, E, Falkard, B, et al. (2009) Oleic acid biosynthesis in Plasmodium falciparum: Characterization of the stearoyl-CoA desaturase and investigation as a potential therapeutic target. PLoS One 4, e6889.CrossRefGoogle ScholarPubMed
Gregory, TR (2020) Animal Genome Size Database. In: Genome Size http://www.genomesize.com. Accessed 18 October 2020Google Scholar
Hashimoto, K, Yoshizawa, AC, Okuda, S, Kuma, K, Goto, S and Kanehisa, M (2008) The repertoire of desaturases and elongases reveals fatty acid variations in 56 eukaryotic genomes. Journal of Lipid Research 49, 183–191.CrossRefGoogle ScholarPubMed
Hatcher, MJ, Dick, JT and Dunn, AM (2012) Diverse effects of parasites in ecosystems: Linking interdependent processes. Frontiers in Ecology and the Environment 10, 186–194.CrossRefGoogle Scholar
Hotez, PJ, Brindley, PJ, Bethony, JM, King, CH, Pearce, EJ and Jacobson, J (2008) Helminth infections: The great neglected tropical diseases. Journal of Clinical Investigations 118, 1311–1321.CrossRefGoogle ScholarPubMed
Howe, KL, Bolt, BJ, Shafie, M, Kersey, P and Berriman, M (2017) Wormbase ParaSite − a comprehensive resource for helminth genomics. Molecular and Biochemical Parasitology 215, 2–10.CrossRefGoogle ScholarPubMed
International Helminth Genomes Consortium (2019) Comparative genomics of the major parasitic worms. Nature Genetics 51, 163.CrossRefGoogle Scholar
Johnson, PTJ, Dobson, A, Lafferty, KD, Marcogliese, DJ, Memmott, J, Orlofske, SA, Poulin, R and Thieltges, DW (2010) When parasites become prey: Ecological and epidemiological significance of eating parasites. Trends in Ecology & Evolution 25, 362–371.CrossRefGoogle ScholarPubMed
Kabeya, N, Fonseca, MM, Ferrier, DEK, Navarro, JC, Bay, LK, Francis, DS, Tocher, DR, Castro, FC and Monroig, Ó (2018) Genes for de novo biosynthesis of omega-3 polyunsaturated fatty acids are widespread in animals. Science Advances 4, eaar6849.CrossRefGoogle Scholar
Kainz, M, Arts, MT and Mazumder, A (2004) Essential fatty acids in the planktonic food web and their ecological role for higher trophic levels. Limnology and Oceanography 49, 1784–1793.CrossRefGoogle Scholar
Karasov, WH and Martinez del Rio, C (2007) Physiological ecology: How animals process energy, nutrients, and toxins. 741 pp. Princeton, New Jersey, Princeton University Press.CrossRefGoogle Scholar
Khozin-Goldberg, I, Iskandarov, U and Cohen, Z (2011) LC-PUFA from photosynthetic microalgae: Occurrence, biosynthesis, and prospects in biotechnology. Applied Microbiology and Biotechnology 91, 905–915.CrossRefGoogle ScholarPubMed
Knapp, J, Nakao, M, Yanagida, T, Okamoto, M, Saarma, U, Lavikainen, A and Ito, A (2011) Phylogenetic relationships within Echinococcus and Taenia tapeworms (Cestoda: Taeniidae): An inference from nuclear protein-coding genes. Molecular Phylogenetics and Evolution 61, 628–638.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.CrossRefGoogle ScholarPubMed
Kuris, A (1990) Guild structure of larval trematodes in molluscan hosts: Prevalence, dominance and significance of competition. pp. 69–100 in Esch, GW, Bush, AO, Aho, JM (Eds) Parasite communities: Patterns and process. London, Chapman and Hall.CrossRefGoogle Scholar
Kuris, AM, Hechinger, RF, Shaw, JC, et al. (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515–518.CrossRefGoogle ScholarPubMed
Lafferty, KD, Allesina, S, Arim, M, et al. (2008) Parasites in food webs: The ultimate missing links. Ecology Letters 11, 533–546.CrossRefGoogle ScholarPubMed
Lavikainen, A, Haukisalmi, V, Lehtinen, MJ, Henttonen, H, Oksanen, A and Meri, S (2008) A phylogeny of members of the family Taeniidae based on the mitochondrial cox1 and nad1 gene data. Parasitology 135, 1457–1467.CrossRefGoogle ScholarPubMed
Letunic, I, Doerks, T and Bork, P (2015) SMART: Recent updates, new developments and status in 2015. Nucleic Acids Research 43, D257–D260.CrossRefGoogle ScholarPubMed
Machado-Pinto, J and Laborne, L (2016) Cestodes. pp. 421 in Tyring, SK, Lupi, O, UR, Hengge (Eds) Tropical dermatology. Edinburgh, Elsevier.Google Scholar
Marcogliese, DJ (2005) Parasites of the superorganism: Are they indicators of ecosystem health? International Journal for Parasitology 35, 705–716.CrossRefGoogle ScholarPubMed
Marcogliese, DJ and Cone, DK (1997) Food webs: A plea for parasites. Trends in Ecology & Evolution 12, 320–325.CrossRefGoogle ScholarPubMed
Martin, RJ, Robertson, AP and Bjorn, H (1997) Target sites of anthelmintics. Parasitology 114, 111–124.CrossRefGoogle ScholarPubMed
Martín-Durán, JM, Ryan, JF, Vellutini, BC, Pang, K and Hejnol, A (2017) Increased taxon sampling reveals thousands of hidden orthologs in flatworms. Genome Research 27, 1263–1272.CrossRefGoogle ScholarPubMed
McKee, KM, Koprivnikar, J, Johnson, PTJ and Arts, MT (2020) Parasite infectious stages provide essential fatty acids and lipid-rich resources to freshwater consumers. Oecologia 192, 477–488.CrossRefGoogle ScholarPubMed
Min, XJ and Hickey, DA (2007) DNA asymmetric strand bias affects the amino acid composition of mitochondrial proteins. DNA Research 14, 201–206.CrossRefGoogle ScholarPubMed
Minematsu, T, Yamazaki, S, Uji, Y, Okabe, H, Korenaga, M and Tada, I (1990) Analysis of polyunsaturated fatty acid composition of Strongyloides ratti in relation to development. Journal of Helminthology 64, 303–309.CrossRefGoogle ScholarPubMed
Mironova, E, Gopko, M, Pasternak, A, Mikheev, V and Taskinen, J (2019) Trematode cercariae as prey for zooplankton: Effect on fitness traits of predators. Parasitology 146, 105–111.CrossRefGoogle ScholarPubMed
Monroig, Ó and Kabeya, N (2018) Desaturases and elongases involved in polyunsaturated fatty acid biosynthesis in aquatic invertebrates: A comprehensive review. Fisheries Science 84, 911–928.CrossRefGoogle Scholar
Mora, C, Tittensor, DP, Adl, S, Simpson, AGB and Worm, B (2011) How many species are there on earth and in the ocean? PLoS Biology 9, e1001127.CrossRefGoogle ScholarPubMed
Morley, NJ (2012) Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia 691, 7–19.CrossRefGoogle Scholar
National Center for Biotechnology Information (2020) Taxonomy statistics:txid6157. In: NCBI. https://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi?mode=Info&id=6157&lvl=3&p=has_linkout&p=blast_url&p=genome_blast&p=mapview&lin=f&keep=1&srchmode=1&unlock. Accessed 18 October 2020Google Scholar
Nichols, DS (2003) Prokaryotes and the input of polyunsaturated fatty acids to the marine food web. FEMS Microbiology Letters 219, 1–7.CrossRefGoogle ScholarPubMed
Olson, PD and Tkach, VV (2005) Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Advances in Parasitology 60, 165–243.CrossRefGoogle ScholarPubMed
Ondrejicka, DA, Locke, SA, Morey, K, Borisenko, AV and Hanner, RH (2014) Status and prospects of DNA barcoding in medically important parasites and vectors. Trends in Parasitology 30, 582–591.CrossRefGoogle ScholarPubMed
Orlofske, SA, Jadin, RC and Johnson, PTJ (2015) It's a predator–eat–parasite world: How characteristics of predator, parasite and environment affect consumption. Oecologia 178, 537–547.CrossRefGoogle ScholarPubMed
Park, JK, Kim, KH, Kang, S, Kim, W, Eom, KS and Littlewood, DTJ (2007) A common origin of complex life cycles in parasitic flatworms: Evidence from the complete mitochondrial genome of Microcotyle sebastis (Monogenea: Platyhelminthes). BMC Evolutionary Biology 7, 11.CrossRefGoogle Scholar
Pereira, SL, Leonard, AE and Mukerji, P (2003) Recent advances in the study of fatty acid desaturases from animals and lower eukaryotes. Prostaglandins, Leukotrienes & Essential Fatty Acids 68, 97–106.CrossRefGoogle Scholar
Peyou-Ndi, MM, Watts, JL and Browse, J (2000) Identification and characterization of an animal delta (12) fatty acid desaturase gene by heterologous expression in Saccharomyces cerevisiae. Archives of Biochemistry and Biophysics 376, 399–408.CrossRefGoogle ScholarPubMed
Pottinger, PS and Jong, EC (2017) Trematodes. pp. 664 in Sanford, CA, Jong, EC, PS, Pottinger (Eds) The travel and tropical medicine manual. Edinburgh, Elsevier Health Sciences.Google Scholar
Poulin, R and Randhawa, HS (2015) Evolution of parasitism along convergent lines: From ecology to genomics. Parasitology 142, S6–S15.CrossRefGoogle ScholarPubMed
Preston, DL, Orlofske, SA, Lambden, JP and Johnson, PTJ (2013) Biomass and productivity of trematode parasites in pond ecosystems. Journal of Animal Ecology 82, 509–517.CrossRefGoogle ScholarPubMed
Riutort, M, Álvarez-Presas, M, Lázaro, E, Solà, E and Paps, J (2012) Evolutionary history of the Tricladida and the Platyhelminthes: An up-to-date phylogenetic and systematic account. International Journal of Developmental Biology 56, 5–17.CrossRefGoogle ScholarPubMed
Ronquist, F, Teslenko, M, Van Der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Rosenkranz, M, Lagrue, C, Poulin, R and Selbach, C (2018) Small snails, high productivity? Larval output of parasites from an abundant host. Freshwater Biology 63, 1602–1609.CrossRefGoogle Scholar
Schariter, JA, Pachuski, J, Fried, B and Sherma, J (2002) Determination of neutral lipids and phospholipids in the cercariae of Schistosoma mansoni by high performance thin layer chromatography. Journal of Liquid Chromatography & Related Technologies 25, 1615–1622.CrossRefGoogle Scholar
Sievers, F, Wilm, A, Dineen, D, et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using clustal Omega. Molecular Systems Biology 7, 539.CrossRefGoogle ScholarPubMed
Silvestro, D and Michalak, I (2012) raxmlGUI: a graphical front-end for RAxML. Organisms Diversity and Evolution 12, 335–337.CrossRefGoogle Scholar
Smyth, JD and McManus, DP (1989) The physiology and biochemistry of Cestodes. 2nd. Ed. Cambridge, Cambridge Univ. Pr.CrossRefGoogle Scholar
Sperling, P, Ternes, P, Zank, TK and Heinz, E (2003) The evolution of desaturases. Prostaglandins, Leukotrienes & Essential Fatty Acids 68, 73–95.CrossRefGoogle ScholarPubMed
Spychalla, JP, Kinney, AJ and Browse, J (1997) Identification of an animal omega-3 fatty acid desaturase by heterologous expression in Arabidopsis. Proceedings of the National Academy of Sciences 94, 1142–1147.CrossRefGoogle ScholarPubMed
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.CrossRefGoogle ScholarPubMed
Tielens, AG (1997) Biochemistry of trematodes. pp. 309–343 in Fried, B, Graczyk, TK (Eds) Advances in trematode biology. CRC Press. Boca Raton.Google Scholar
Tunholi-Alves, VM, Tunholi, VM, Gôlo, P, Lustrino, D, Maldonado, A, Bittencourt, VREP, Maria de Lurdes, A and Pinheiro, J (2011) Lipid levels in Biomphalaria glabrata infected with different doses of Echinostoma paraensei miracidia. Experimental Parasitology 128, 212–216.CrossRefGoogle ScholarPubMed
Twining, CW, Brenna, JT, Hairston, NG and Flecker, AS (2016) Highly unsaturated fatty acids in nature: What we know and what we need to learn. Oikos 125, 749–760.CrossRefGoogle Scholar
Viney, M (2017) How can we understand the genomic basis of nematode parasitism? Trends in Parasitology 33, 444–452.CrossRefGoogle ScholarPubMed
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