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Chemical and genetic differences between Hawaiian lineages of the alga Asparagopsis taxiformis

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Abstract

Asparagopsis taxiformis is a widely distributed red alga, known locally in Hawai‘i as limu kohu. Over the past decade, it was discovered that A. taxiformis is a multiphyletic species, with analysis of mitochondrial DNA revealing several genetically distinct lineages present around the world. A. taxiformis samples from around O‘ahu, belonging to the three different lineages found in Hawaiian waters, were collected and subjected to parallel genetic and chemical profiling. Sequencing of the mitochondrial cytochrome oxidase I gene clearly separated the three lineages. In parallel, GC-MS profiling of the samples was conducted in order to determine whether there were any accompanying chemical differences. Analysis of the metabolite profiles using a range of multivariate statistical techniques showed that lineage 4 could be readily differentiated from the other two lineages, lineage 1 and lineage 2, by its chemical profile. Several halogenated metabolites characteristic of lineage 4 were also identified, including methyl bromoiodoacetate, methyl tribromoacetate, carbon tetrabromide, and dibromoacetone.

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References

  • Abbott IA (1984) Limu: an ethnobotanical study of some Hawaiian seaweeds. National Tropical Botanical Garden, Lawai, USA

    Google Scholar 

  • Andreakis N, Procaccini G, Kooistra WHCF (2004) Asparagopsis taxiformis and Asparagopsis armata (Bonnemaisoniales, Rhodophyta): genetic and morphological identification of Mediterranean populations. Eur J Phycol 39:273–283

    Article  CAS  Google Scholar 

  • Andreakis N, Kooistra WHCF, Procaccini G (2007) Microsatellite markers in an invasive strain of Asparagopsis taxiformis (Bonnemaisoniales, Rhodophyta): insights in ploidy level and sexual reproduction. Gene 406:144–151

    Article  PubMed  CAS  Google Scholar 

  • Andreakis N, Costello P, Zanolla M, Saunders GW, Mata L (2016) Endemic or introduced? Phylogeography of Asparagopsis (Florideophyceae) in Australia reveals multiple introductions and a new mitochondrial lineage. J Phycol 52:141–147

    Article  PubMed  CAS  Google Scholar 

  • Beissner RS, Guilford WJ, Coates RM, Hager LP (1981) Synthesis of brominated heptanones and bromoform by a bromoperoxidase of marine origin. Biochemistry 20:3724–3731

    Article  PubMed  CAS  Google Scholar 

  • Bolton JJ, Andreakis N, Anderson RJ (2011) Molecular evidence for three separate cryptic introductions of the red seaweed Asparagopsis in South Africa. Afr J Mar Sci 33:263–271

    Article  Google Scholar 

  • Burreson BJ, Moore RE, Roller P (1975) Haloforms in the essential oil of the alga Asparagopsis taxiformis. Tetrahedron Lett 16:473–476

    Article  Google Scholar 

  • Burreson BJ, Moore RE, Roller PP (1976) Volatile halogen compounds in the alga Asparagopsis taxiformis (Rhodophyta). J Agric Food Chem 24:856–861

    Article  CAS  Google Scholar 

  • Dijoux L, Viard F, Payri C (2014) The more we search, the more we find: discovery of a new lineage and a new species complex in the genus Asparagopsis. PLoS One 9:e103826

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fenical W (1974) Polyhaloketones from the red seaweed Asparagopsis taxiformis. Tetrahedron Lett 15:4463–4466

    Article  Google Scholar 

  • Ferreira LDS, Casanova Turatti IC, Lopes NP, Guaratini T, Colepicolo P, Oliveira Filho EC, Garla RC (2012) Apolar compounds in seaweeds from Fernando de Noronha Archipelago (northeastern coast of Brazil). Int J Anal Chem 2012:431954

    PubMed Central  Google Scholar 

  • Genovese G, Tedone L, Hamann MT, Morabito M (2009) The Mediterranean red alga Asparagopsis: a source of compounds against Leishmania. Mar Drugs 7:361–366

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Greff S, Zubia M, Genta-Jouve G, Massi L, Perez T, Thomas OP (2014) Mahorones, highly brominated cyclopentenones from the red alga Asparagopsis taxiformis. J Nat Prod 77:1150–1155

    Article  PubMed  CAS  Google Scholar 

  • Jha B, Kavita K, Westphal J, Hartmann A, Schmitt-Kopplin P (2013) Quorum sensing inhibition by Asparagopsis taxiformis, a marine macro alga: separation of the compound that interrupts bacterial communication. Mar Drugs 11:253–265

    Article  PubMed  PubMed Central  Google Scholar 

  • Knowlton K (1993) Sibling species in the sea. Annu Rev Ecol Syst 24:189–216

    Article  Google Scholar 

  • Kuepper FC, Leblanc C, Meyer-Klaucke W, Potin P, Feiters MC (2014) Different speciation for bromine in brown and red algae, revealed by in vivo X-ray absorption spectroscopic studies. J Phycol 50:652–664

    Article  CAS  Google Scholar 

  • Kurihara A, Horiguchi H, Hanyuda T, Kawai H (2016) Phylogeography of Asparagopsis taxiformis revisited: combined mtDNA data provide novel insights into population structure in Japan. Phycol Res 64:95–101

    Article  Google Scholar 

  • Marshall RA, Harper DB, McRoberts WC, Dring MJ (1999) Volatile bromocarbons produced by Falkenbergia stages of Asparagopsis spp. (Rhodophyta). Limnol Oceanogr 44:1348–1352

    Article  CAS  Google Scholar 

  • Marshall RA, Hamilton JTG, Dring MJ, Harper DB (2003) Do vesicle cells of the red alga Asparagopsis (Falkenbergia stage) play a role in bromocarbon production? Chemosphere 52:471–475

    Article  PubMed  CAS  Google Scholar 

  • Mata L, Gaspar H, Justino F, Santos R (2011) Effects of hydrogen peroxide on the content of major volatile halogenated compounds in the red alga Asparagopsis taxiformis (Bonnemaisoniaceae). J Appl Phycol 23:827–832

    Article  CAS  Google Scholar 

  • Mata L, Wright E, Owens L, Paul N, de Nys R (2013) Water-soluble natural products from seaweed have limited potential in controlling bacterial pathogens in fish aquaculture. J Appl Phycol 25:1963–1973

    Article  CAS  Google Scholar 

  • Mata L, Lawton RJ, Magnusson M, Andreakis N, de Nys R, Paul NA (2017) Within-species and temperature-related variation in the growth and natural products of the red alga Asparagopsis taxiformis. J Appl Phycol 29:1437–1447

    Article  CAS  Google Scholar 

  • McConnell O, Fenical W (1977) Halogen chemistry of the red alga Asparagopsis. Phytochemistry 16:367–374

    Article  CAS  Google Scholar 

  • Ni Chualain F, Maggs CA, Saunders GW, Guiry MD (2004) The invasive genus Asparagopsis (Bonnemaisoniaceae, Rhodophyta): molecular systematics morphology and ecophysiology of Falkenbergia isolates. J Phycol 40:1112–1126

    Article  Google Scholar 

  • Ohsawa N, Ogata Y, Okada N, Itoh N (2001) Physiological function of bromoperoxidase in the red marine alga, Corallina pilulifera: production of bromoform as an allelochemical and the simultaneous elimination of hydrogen peroxide. Phytochemistry 58:683–692

    Article  PubMed  CAS  Google Scholar 

  • Padilla-Gamino JL, Carpenter RC (2007) Seasonal acclimatization of Asparagopsis taxiformis (Rhodophyta) from different biogeographic regions. Limnol Oceanogr 52:833–842

    Article  Google Scholar 

  • Paul C, Pohnert G (2011) Production and role of volatile halogenated compounds from marine algae. Nat Prod Rep 28:186–195

    Article  PubMed  CAS  Google Scholar 

  • Paul NA, de Nys R, Steinberg PD (2006a) Chemical defence against bacteria in the red alga Asparagopsis armata: linking structure with function. Mar Ecol Prog Ser 306:87–101

    Article  CAS  Google Scholar 

  • Paul NA, de Nys R, Steinberg PD (2006b) Seaweed-herbivore interactions at a small scale: direct tests of feeding deterrence by filamentous algae. Mar Ecol Prog Ser 323:1–9

    Article  Google Scholar 

  • Pedersen M, Collén J, Abrahamsson K, Ekdahl A (1996) Production of halocarbons from seaweeds: an oxidative stress reaction? Sci Mar 60(S1):257–263

    CAS  Google Scholar 

  • Ragonese C, Tedone L, Beccaria M, Torre G, Cichello F, Cacciola F, Dugo P, Mondello L (2014) Characterisation of lipid fraction of marine macroalgae by means of chromatography techniques coupled to mass spectrometry. Food Chem 145:932–940

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406

    PubMed  CAS  Google Scholar 

  • Saunders GW (2005) Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philos Trans R Soc B 360:1879–1888

    Article  CAS  Google Scholar 

  • Sherwood AR (2008) Phylogeography of Asparagopsis taxiformis (Bonnemaisoniales, Rhodophyta) in the Hawaiian islands: two mtDNA markers support three separate introductions. Phycologia 47:79–88

    Article  CAS  Google Scholar 

  • Sherwood AR, Sauvage T, Kurihara A, Conklin KY, Presting GG (2010) A comparative analysis of COI, LSU and UPA marker data for the Hawaiian florideophyte Rhodophyta: implications for DNA barcoding of red algae. Cryptogam Algol 31:451–465

    Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    PubMed  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Theiler R, Cook JC, Hager LP, Siuda JF (1978) Halohydrocarbon synthesis by bromoperoxidase. Science 202:1094–1096

    Article  PubMed  CAS  Google Scholar 

  • Vedhagiri K, Manilal A, Valliyammai T, Shanmughapriya S, Sujith S, Selvin J, Natarajaseenivasan K (2009) Antimicrobial potential of a marine seaweed Asparagopsis taxiformis against Leptospira javanica isolates of rodent reservoirs. Ann Microbiol 59:431–437

    Article  CAS  Google Scholar 

  • Wolk CP (1968) Role of bromine in formation of refractile inclusions of vesicle cells of Bonnemaisoniaceae (Rhodophyta). Planta 78:371–378

    Article  PubMed  CAS  Google Scholar 

  • Woolard FX, Moore RE, Roller PP (1976) Halogenated acetamides, but-3-en-2-ols, and isopropanols from Asparagopsis taxiformis (Delile) Trev. Tetrahedron 32:2843–2846

    Article  CAS  Google Scholar 

  • Woolard FX, Moore RE, Roller PP (1979) Halogenated acetic and acrylic acids from the red alga Asparagopsis taxiformis. Phytochemistry 18:617–620

    Article  CAS  Google Scholar 

  • Zanolla M, Carmona R, De la Rosa J, Salvador N, Sherwood AR, Andreakis N, Altamirano M (2014) Morphological differentiation of cryptic lineages within the invasive genus Asparagopsis (Bonnemaisoniales, Rhodophyta). Phycologia 53:233–242

    Article  Google Scholar 

  • Zanolla M, Altamirano M, Carmona R, De la Rosa J, Souza-Egipsy V, Sherwood A, Tsiamis K, Barbosa AM, Roman Munoz A, Andreakis N (2018) Assessing global range expansion in a cryptic species complex: insights from the red seaweed genus Asparagopsis (Florideophyceae). J Phycol 54:12–24

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This project is supported in part by the NSF Hawai‘i EPSCoR Program under National Science Foundation Award EPS-0903833 and by the College of Pharmacy, University of Hawai‘i at Hilo.

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Correspondence to Robert P. Borris.

Additional information

Jerry L. M. Kaluhiwa died before publication of this work was completed.

Electronic supplementary material

ESM 1

Included as supporting information are tables with additional data on sample collection locations and on the MS data of metabolites, a figure illustrating collection locations, a figure illustrating the characteristic differences between the three lineages found in Hawai‘i, and a heatmap analysis showing clustering of both samples and compounds. (PDF 817 kb)

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Clark, B.R., Mizobe, M., Kaluhiwa, J.L.M. et al. Chemical and genetic differences between Hawaiian lineages of the alga Asparagopsis taxiformis. J Appl Phycol 30, 2549–2559 (2018). https://doi.org/10.1007/s10811-018-1474-6

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  • DOI: https://doi.org/10.1007/s10811-018-1474-6

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