Haslea nusantara (Bacillariophyceae), a new blue diatom from the Java Sea, Indonesia: morphology, biometry and molecular characterization
Cover of volume 152, number 2 of Plant Ecology and Evolution
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Keywords

Indonesia
Bacillariophyceae
blue diatoms
Haslea
molecular phylogeny
genomic study

How to Cite

Prasetiya, F., Gastineau, R., Poulin, M., Lemieux, C., Turmel, M., Syakti, A., Hardivillier, Y., Widowati, I., Risjani, Y., Iskandar, I., Subroto, T., Falaise, C., Arsad, S., Safitri, I., Mouget, J.-L. and Leignel, V. (2019) “Haslea nusantara (Bacillariophyceae), a new blue diatom from the Java Sea, Indonesia: morphology, biometry and molecular characterization”, Plant Ecology and Evolution, 152(2), pp. 188-202. doi: 10.5091/plecevo.2019.1623.

Abstract

Background and aims – The present study aims to describe a new species of pennate blue diatom from the genus Haslea, H. nusantara sp. nov., collected from Semak Daun Island, the Seribu Archipelago, in Indonesian marine waters.

Methods – Assessment for species identification was conducted using light microscopy, Scanning Electron Microscopy and molecular techniques. The morphological characteristics of H. nusantara have been described, illustrated and compared to other morphologically similar blue Haslea taxa, distributed worldwide. Additionally, molecular characterization was achieved by sequencing plastidial and mitochondrial genomes.

Key results – This new species, named Haslea nusantara, cannot be discriminated by its morphology (stria density) but it is characterized by its gene sequences (rbcL chloroplast gene and cox1 mitochondrial gene). Moreover, it differentiates from other blue Haslea species by the presence of a thin central bar, which has been previously reported in non-blue species like H. pseudostrearia. The complete mitochondrion (36,288 basepairs, bp) and plastid (120,448 bp) genomes of H. nusantara were sequenced and the gene arrangements were compared with other diatom genomes. Phylogeny analyses established using rbcL indicated that H. nusantara is included in the blue Haslea cluster and close to a blue Haslea sp. found in Canary Islands (H. silbo sp. ined.).

Conclusions – All investigations carried out in this study show that H. nusantara is a new blue-pigmented species, which belongs to the blue Haslea clade, with an exceptional geographic distribution in the Southern Hemisphere.

https://doi.org/10.5091/plecevo.2019.1623
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References

An S.M., Noh J.H., Choi D.H., Lee J.H., Yang E.C. (2016) Repeat region absent in mitochondrial genome of tube-dwelling diatom Berkeleya fennica (Naviculales, Bacillariophyceae). Mitochondrial DNA Part A 27: 2137–2138. https://doi.org/10.3109/19401736.2014.982594

An S.M., Kim S.Y., Noh J.H., Yang E.C. (2017) Complete mitochondrial genome of Skeletonema marinoi (Mediophyceae, Bacillariophyta), a clonal chain forming diatom in the west coast of Korea. Mitochondrial DNA Part A 28: 19–20. https://doi.org/10.3109/19401736.2015.1106523

Boisvert S., Raymonf F., Godzaridis E., Laviolette F., Corbeil J. (2012) Ray Meta: scalable de novo metagenome assembly and profiling. Genome Biology R122: 1–13. https://doi.org/ 0.1186/gb-2012-13-12-r122

Bramburger A., Hamilton P.B. (2014) Effects of a simulated upwelling event on the littoral epilithic diatom community of an ancient tropical lake (Lake Matano, Sulawesi Island, Indonesia). Hydrobiologia 739: 133–143. https://doi.org/10.1007/s10750-013-1598-2

Bramburger A.J., Hamilton P.B., Hehanussa P.E., Haffner G.D. (2008) Processes regulating the community composition and relative abundance of taxa in the diatom communities of the Malili Lakes, Sulawesi Island, Indonesia. Hydrobiologia 615: 215–224. https://doi.org/10.1007/978-1-4020-9582-5_15

Cao M., Yuan X-L., Bi G. (2016) Complete sequence and analysis of plastid genomes of Pseudo-nitzschia multiseries (Bacillariophyta). Mitochondrial DNA Part A 27: 2897–2898. https://doi.org/10.3109/19401736.2015.1060428

Cardinal A., Poulin M., Berard-Therriault L. (1984) Les diatomées benthiques de substrats durs des eaux marines et saumâtres du Québec. 4. Naviculales, Naviculaceae (à l’exclusion des genres Navicula, Donkinia, Gyrosigma et Pleurosigma). Le Naturaliste canadien 111: 369–394.

Darling A.E., Mau B., Perna N.T. (2010) ProgressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5: e11147. https://doi.org/10.1371/journal.pone.0011147

Doyle J.J., Doyle J.L. (1990) Isolation of plant DNA from fresh tissue. Focus 12: 13–15.

Evers H., 2016 - Nusantara: history of a concept. Journal of Malaysian Branch of the Royal Asiatic Society 89: 3–14. https://doi.org/10.1353/ras.2016.0004

Falkowski P.G., KatZ M.E., Knoll A.H., Quigg A., Raven J.A., Schofield O., Taylor F.J.R. (2004) The evolution of modern eukaryotic phytoplankton. Science 305: 354–360. https://doi.org/10.1126/science.1095964

Gagnon J. (2004) Création d’outils pour l’automatisation d’analyses phylogénétiques de génomes d’organites. PhD thesis, Université Laval, Quebec City, Canada.

Gaillon B. (1820) Des huîtres vertes, et des causes de cette coloration. Journal de Physique, de Chimie, d’Histoire Naturelle et des Arts 91: 222–225.

Galachyants Y.P., Morozov A.A., Mardanov A.V., Beletsky A.V., Ravin N.V., Petrova D.P., Likhoshway Y.V. (2012) Complete chloroplast genome sequence of freshwater araphid pennate diatom alga Synedra acus from Lake Baikal. International Journal of Biology 4: 27–35. https://doi.org/10.5539/ijb.v4n1p27

Gastineau R. (2011) Biodiversité, reproduction et phylogénie des diatomées bleues du genre Haslea et valorisation de leurs pigments de type marennine. PhD thesis, Université du Maine, Le Mans, France.

Gastineau R., Pouvreau J.B., Hellio C., Morançais M., Fleurence J., Gaudi P., Bourgougnon N., Mouget J.-L. (2012a) Biological activities of purified marennine, the blue pigment responsible for the greening of oysters. Journal of Agricultural and Food Chemistry 60: 3599–3605. https://doi.org/10.1021/jf205004x

Gastineau R., Davidovich N.A., Bardeau J.-F., Caruso A., Leignel V., Hardivillier Y., Jacquette B., Davidovich O.I., Rincé Y., Gaudin P., Cox E.J., Mouget J.-L. (2012b) Haslea karadagensis (Bacillariophyta): a second blue diatom, recorded from the Black Sea and producing a novel blue pigment. European Journal of Phycology 47: 469–479. https://doi.org/10.1080/09670262.2012.741713

Gastineau R., Turcotte F., Pouvreau J.B., Morançais M., Fleurence J., Windarto E., Prasetyia F.S., Arsad S., Jaouen P., Babin M., Coiffard L., Couteau C., Bardeau J.-F., Jacquette B., Leignel V., Hardivillier Y., Marcotte I., Bourgougnon N., Tremblay R., Deschênes J.-S., Badawy H., Pasetto P., Davidovich N., Hansen G., Dittmer J., Mouget J.-L. (2014a) Marennine, promising blue pigments from a widespread Haslea diatom species complex. Marine Drugs 12: 3161–3189. https://doi.org/10.3390/md12063161

Gastineau R., HardivillierA Y., Leignel V., Tekaya N., Morançais M., Fleurence J., Davidovich N., Jacquette B., Gaudin P., Hellio C., Bourgougnon N., Mouget J.-L. (2014b) Greening effect on oysters and biological activities of the bleu pigments produced by the diatom Haslea karadagensis (Naviculaceae). Aquaculture 368/369: 61–67. https://doi.org/10.1021/jf205004x

Gastineau R., Hansen G., Davidovich N.A., Davidovich O., Bardeau J.-F., Kaczmarska I., Ehrman J.M., Leignel V., Hardivillier Y., Jacquette B., Poulin M., Morançais M., Fleurence J., Mouget J.-L. (2016) A new blue-pigmented hasleoid diatom, Haslea provincialis, from the Mediterranean Sea. European Journal of Phycology 51: 156–170. https://doi.org/10.1080/09670262.2015.1110861

Guiry M.D. , Guiry G.M. (2018) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available from http://www.algaebase.org [accessed 1 Sep. 2018].

Hendrarto B., Nitisuparjo M. (2011) Biodiversity of benthic diatom and primary productivity of benthic micro-flora in mangrove forest on central Java. Journal of Coastal Development 14: 131–140.

Kaczmarska I., Legresley M.M., Martin J.L., Ehrman J. (2005) Diversity of the diatom genus Pseudo-nitzschia Peragallo in the Quoddy region of the Bay of Fundy, Canada. Harmful Algae 4: 1–19. https://doi.org/10.1016/j.hal.2003.07.001

Kumar S., Stecher G., Tamura K. (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874. https://doi.org/10.1093/molbev/msw054

Lankester E.R. (1886) On green oysters. Quarterly Journal of Microscopical Science 26: 1–94.

Li Y., Chen X., Sun Z., Xu K. (2017) Taxonomy and molecular phylogeny of three marine benthic species of Haslea (Bacillariophyceae), with transfer of two species to Navicula. Diatom Research: 451–463. https://doi.org/10.1080/0269249X.2017.1401008

Lohse M., Drechsel O., Bock R. (2007) OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Current Genetics 52: 267–274. https://doi.org/10.1007/s00294-007-0161-y

Massé G., Rincé Y., Cox E.J., Allard G., Belt S.T., Rowland S.J. (2001) Haslea salstonica sp. nov. and Haslea pseudostrearia sp. nov. (Bacillariophyta), two new epibenthic diatoms from the Kingsbridge Estuary, United Kingdom. Sciences de la vie/Life Sciences 324: 617–626. https://doi.org/10.1016/S0764-4469(01)01330-0

Mouget J.-L., Gastineau R., Davidovich O., Gaudin P., Davidovich N.A. (2009) Light is a key factor in triggering sexual reproduction in the pennate diatom Haslea ostrearia. FEMS Microbiology and Ecology 69: 194–201. https://doi.org/10.1111/j.1574-6941.2009.00700.x

Oudot-Le Secq M.P., Grimwood J., Shapiro H., Armbrust E.V., Bowler C., Green B.R. (2007) Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: comparison with other plastid genomes of the red lineage. Molecular Genetics and Genomics 277: 427–439. https://doi.org/10.1007/s00438-006-0199-4

Oudot-Le Secq M.P., Green B.R. (2011) Complex repeat structures and novel features in the mitochondrial genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana. Gene 476: 20–26. https://doi.org/10.1016/j.gene.2011.02.001

Palinska K.A., Surosz W. (2018) A bleu-pigmented hasleoid diatom, Haslea sp., from the Adriatic Sea. Oceanological and Hydrobiological Studies 47: 60–66. https://doi.org/10.1515/ohs-2018-0007

Pillet L., Vargas C., Pawlowski J. (2011) Molecular Identification of Sequestered Diatom Chloroplasts and Kleptoplastidy in Foraminifera. Protist 162: 394–404. https://doi.org/10.1016/j.protis.2010.10.001

Pogoda C.S., Keepers K.G., Hamsher S.E., Stepanek J.G., Kane N.C., Kociolek J.P. (2018) Comparative analysis of the mitochondrial genomes of six newly sequenced diatoms reveals group II introns in the barcoding region of cox1. Mitochondrial DNA Part A 11: 1–9. https://doi.org/10.1080/24701394.2018.1450397

Poulin M., Massé G., Belt S.T., Delavault P., Rousseau F., Robert J.-M., Rowland S.J. (2004) Morphological, biochemical and molecular evidence for the transfer of Gyrosigma nipkowii Meister to the genus Haslea (Bacillariophyta). European Journal of Phycology 39: 181–195. https://doi.org/10.1080/0967026042000202136

Poulin M., Méléder V., Mouget J.-L. (2019) Typification of the first recognized blue pigmented diatom, Haslea ostrearia (Bacillariophyceae). Plant Ecology and Evolution 152: 402–408. https://doi.org/10.5091/plecevo.2019.1622

Pouvreau J.B., Morançais M., Massé G., Rosa P., Robert J.-M., Fleurence J., Pondaven P. (2006a) Purification of the blue-green pigment “marennine” from the marine tychopelagic diatom Haslea ostrearia (Gaillon/Bory) Simonsen. Journal of Applied Phycology 18: 769–781. https://doi.org/10.1007/s10811-006-9088-9

Pouvreau J.B., Morançais M., Fleury F., Rosa P., Thion L., Cahingt B., Zal F., Fleurence J., Pondaven P. (2006b) Preliminary characterization of the blue-green pigment “marennine” from the marine tychopelagic diatom Haslea ostrearia (Gaillon/Bory) Simonsen. Journal of Applied Phycology 18: 757–767. https://doi.org/10.1007/s10811-006-9087-x

Pouvreau J.B., Housson E., Le Tallec L., Morançais M., Rincé Y., Fleurence J., Pondaven P. (2007a) Growth inhibition of several marine diatom species induced by the shading effect and allelopathic activity of marennine, a blue-green polyphenolic pigment of the diatom Haslea ostrearia (Gaillon/Bory) Simonsen. Journal of Experimental Marine Biology and Ecology 352: 212–225. https://doi.org/10.1016/j.jembe.2007.07.011

Pouvreau J.B., Morançais M., Fleurence J., Pondaven P. (2007b) Method for the quantification of the blue-green pigment “marennine” synthesized by the marine diatom Haslea ostrearia (Gaillon/Bory) Simonsen using HPLC gel-filtration and photodiode-array detection. Journal of Applied Phycology 19: 263–270. https://doi.org/10.1007/s10811-006-9133-8

Pouvreau J.B., Morançais M., Taran F., Rosa P., Dufossé L., Guépard F., Pin S., Fleurence J., Pondaven P. (2008) Antioxidant and free radical scavenging properties of marennine, a blue-green polyphenolic pigment from the diatom Haslea ostrearia (Gaillon/Bory) Simonsen responsible for the natural greening of cultured oysters. Journal of Agricultural and Food Chemistry 56: 6278–6286. https://doi.org/10.1021/jf073187n

Prasetiya F.S., Safitri I., Widowati I., Cognie B., Decottignies P., Gastineau R., Morançais M., Windarto E., Tremblay R., Mouget J.-L. (2016) Does allelopathy affect co-culturing Haslea ostrearia with other microalgae relevant to aquaculture? Journal of Applied Phycology 28: 2241–2254. https://doi.org/10.1007/s10811-015-0779-y

QGIS Development Team (2018) QGIS Geographic Information System. Open Source Geospatial Foundation Project. Available from https://www.qgis.org [accessed 1 Sep. 2018].

Ravin N.V., Galahyants Y.P., Mardanov A.V., Beletsky A.V., Petrova D.P., Sherbakova T.A., Zakharova Y.R., Likhoshway Y.V., Skyabin K.G., Grachev M.A. (2010) Complete sequence of the mitochondrial genome of a diatom alga Synedra acus and comparative analysis of diatom mitochondrial genomes. Current Genetics 56: 215–223. https/doi.org/10.1007/s00294-010-0293-3

Roberts C.M., Mittermeier C.G., Schueler F.W. (2006) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295: 1280–1284. https://doi.org/10.1126/science.1067728

Ruck E.C., Nakov T., Jansen R.K., Theriot E.C., Alverson A.J. (2014) Serial gene losses and foreign DNA underlie size and sequence variation in the plastid genomes of diatoms. Genome Biology and Evolution 6: 644–654. https://doi.org/10.1093/gbe/evu039

Simonsen R. (1974) The diatom plankton of the India Ocean Expedition of RV Meteor 1964–1965. ’Meteor’ Forschungsergebnisse Rehe D 19: 1–107.

Sprat T. (1669) The history of the generation and ordering of green oysters, commonly called Colchester oysters. History of Royal Society of London. In: Sprat T., Cowley A. (eds) The history of the Royal-Society of London for the improving of natural knowledge by Tho. Sprat: 307–319. Oxford, Martyn & Allestry.

Stamatakis A., Hoover P., Rougemont J. (2008) A rapid bootstrap algorithm for the RAxML web-servers. Systematic Biology 75: 758–771. https://doi.org/10.1080/10635150802429642

Sterrenburg F.A.S., Eeftemeijer P.L.A., Nienhuis P.H. (1995) Diatoms as epiphytes on seagrasses in South Sulawesi (Indonesia) comparison with growth on inert substrata. Botanica Marina 38: 1–7. https://doi.org/10.1515/botm.1995.38.1-6.1

Swofford D.L. (1998) PAUP. Phylogenetic analysis using parsimony (and other methods). Version 4. Sinauer Associates. Smithsonian Institution, Sunderland, Massachusetts.

Talgatti D., Sar E.A., Torgan L.C. (2014) Haslea sigma (Naviculaceae, Bacillariophyta) a new sigmoid benthic species from salt marshes of Southern Brazil. Phytotaxa 177: 231–238. https://doi.org/10.11646/phytotaxa.177.4.4

Tanaka T., Fukuda Y., Yoshino T., Maeda Y., Muto M., Matsumoto M., Mayama S., Matsunaga T. (2011) High-throughput pyrosequencing of the chloroplast genome of a high neutral-lipid-producing marine pennate diatom, Fistulifera sp. strain JPCC DA0580. Photosynthesis Research 109: 223–229. https://doi.org/10.1007/s11120-011-9622-8

Tang X., Bi G. (2016) Complete mitochondrial genome of Fistulifera solaris (Bacillariophycidae). Mitochondrial DNA Part A 27: 4405–4406. https://doi.org/10.3109/19401736.2015.1089545

Turmel M., Lemieux C. (2018) Evolution of the plastid genome in green algae. Advances in Botanical Research 85: 157–193. https://doi.org/10.1016/bs.abr.2017.11.010

Turmel M., Otis C., Lemieux C. (2015) Dynamic evolution of the chloroplast genome in the green algal classes Pedinophyceae and Trebouxiophyceae. Genome Biology and Evolution 7: 2062–2082. https://doi.org/10.1093/gbe/evv130

Villain A., Kojadinovic M., Puppo C., Prioretti L., Hubert P., Zhang Y., Grégori G., Roulet A., Roques C., Claverie J.-M., Gontero B., Blanc G. (2017) Complete mitochondrial genome sequence of the freshwater diatom Asterionella formosa. Mitochondrial DNA Part B 2: 97–98. https://doi.org/10.1080/23802359.2017.1285210

Yuan X.-L., Cao M., Bi G.-Q. (2016) The complete mitochondrial genome of Pseudo-nitzschia multiseries (Bacillariophyta). Mitochondrial DNA Part A 27: 2777–2778. https://doi.org/10.3109/19401736.2015.10530611

Yu M., Ashworth M.P., Hajrah N.H., Khiyami M.A., Sabir M.J., Alhebshi A.M., Jansen R.K. (2018) Evolution of the plastid genomes in diatoms. Advances in Botanical Research 85: 129–155. https://doi.org/10.1016/bs.abr.2017.11.009

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