brown algae; cox2; eastern; hyphochytrids; infection; lsu rrna; mediterranean sea; of the publisher; oomycetes; pathogens; permitted without written consent; phylogeny; resale or republication not; ssu rrna
Abstract :
[en] For the Mediterranean Sea, and indeed most of the world's oceans, the biodiversity and biogeography of eukaryotic pathogens infecting marine macroalgae remains poorly known, yet their ecological impact is probably significant. Based on 2 sampling campaigns on the Greek island of Lesvos in 2009 and 1 in northern Greece in 2012, this study provides first records of 3 intracellular eukaryotic pathogens infecting filamentous brown algae at these locations: Eurychasma dicksonii, Anisolpidium sphacellarum, and A. ectocarpii. Field and microscopic observations of the 3 pathogens are complemented by the first E. dicksonii large subunit ribosomal RNA (LSU rRNA) gene sequence analyses of isolates from Lesvos and other parts of the world. The latter highlights the monophyly of E. dicksonii worldwide and confirms the basal position of this pathogen within the oomycete lineage (Peronosporomycotina). The results of this study strongly support the notion that the geographic distribution of the relatively few eukaryotic seaweed pathogens is probably much larger than previously thought and that many of the world's marine bioregions remain seriously undersampled and understudied in this respect.
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Strittmatter, Martina
Gachon, Claire M. M.
Müller, Dieter G.
Kleinteich, Julia ; Université de Liège - ULiège > Département des sciences de la vie > Physiologie et génétique bactériennes
Heesch, Svenja
Tsirigoti, Amerssa
Katsaros, Christos
Kostopoulou, Maria
Küpper, Frithjof C.
Language :
English
Title :
Intracellular eukaryotic pathogens in brown macroalgae in the Eastern Mediterranean, including LSU rRNA data for the oomycete Eurychasma dicksonii .
Andreou D, Arkush KD, Guégan JF, Gozlan RE (2012) Introduced pathogens and native freshwater biodiversity: a case study of Sphaerothecum destruens. PLoS ONE 7: e36998
Beakes GW, Glockling SL, Sekimoto S (2012) The evolutionary phylogeny of the oomycete 'fungi'. Protoplasma 249: 3-19
Boudouresque CF, Verlaque M (2002) Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar Pollut Bull 44: 32-38
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540-552
Chambouvet A, Morin P, Marie D, Guillou L (2008) Control of toxic marine dinoflagellate blooms by serial parasitic killers. Science 322: 1254-1257
Cook KL, Hudspeth DSS, Hudspeth MES (2001) A cox2 phylogeny of representative marine Peronosporomycetes (Oomycetes). Nova Hedwigia Beih 122: 231-243
Dick MW (2001) Straminipilous fungi. Systematics of the Peronosporomycetes including accounts of the marine straminipilous protists, the plamodiophorids and similar organisms. Kluwer Academic Publishers, Dordrecht
Ercegovic A (1955) Contribution à la connaissance des ectocarpes (Ectocarpus) de l'adriatique moyenne. Acta Adriat 7: 1-74
Gachon CMM, Strittmatter M, Müller DG, Kleinteich J, Küpper FC (2009) Detection of differential host susceptibility to the marine oomycete pathogen Eurychasma dicksonii by real-time PCR: Not all algae are equal. Appl Environ Microbiol 75: 322-328
Gachon CMM, Sime-Ngando T, Strittmatter M, Chambouvet A, Kim GH (2010) Algal diseases: spotlight on a black box. Trends Plant Sci 15: 633-640
Garcias-Bonet N, Sherman T, Duarte C, Marbà N (2011) Distribution and pathogenicity of the protist Labyrinthula sp. in western Mediterranean seagrass meadows. Estuar Coasts 34: 1161-1168
Giaccone G, Bryce Derni C (1971) Informazioni tassonomiche di elementi morfologici ed ecologici di stadi ectocarpoidi presenti sulle coste italiane. Atti Ist Veneto Sci Lett Arti 130: 39-81
Gleason FH, Küpper FC, Amon JP, Picard K and others (2011) Zoosporic true fungi in marine ecosystems: a review. Mar Freshw Res 62: 383-393
Hakariya M, Hirose D, Tokumasu S (2009) Molecular phylogeny of terrestrial holocarpic endoparasitic perono sporomycetes, Haptoglossa spp., inferred from 18s rDNA. Mycoscience 50: 130-136
Hauck F (1878) Notiz über Rhizophydium dicksonii Wright. Österr Bot Z 28: 321
Hausner G, Belkhiri A, Klassen GR (2000) Phylogenetic analysis of the small subunit ribosomal RNA gene of the hyphochytrid Rhizidiomyces apophysatus. Can J Bot 78: 124-128
Ibelings BW, Gsell AS, Mooij WM, Van Donk E, Van Den Wyngaert S, De Senerpont Domis LN (2011) Chytrid infections and diatom spring blooms: paradoxical effects of climate warming on fungal epidemics in lakes. Freshw Biol 56: 754-766
Karling J (1943) The life history of Anisolpidium ectocarpii gen. nov. et sp. nov., and a synopsis and classification of other fungi with anteriorly uniflagellate zoospores. Am J Bot 30: 637-648
Katsaros CI (1995) Apical cells of brown algae with particular reference to Sphacelariales, Dictyotales and Fucales. Phycological Res 43: 43-59
Katsaros C, Karyophyllis D, Galatis B (2006) Cytoskeleton and morphogenesis in brown algae. Ann Bot (Lond) 97: 679-693
Klochkova T, Shim J, Hwang M, Kim G (2012) Host-parasite interactions and host species susceptibility of the marine oomycete parasite, Olpidiopsis sp., from Korea that infects red algae. J Appl Phycol 24: 135-144
Küpper FC, Müller DG (1999) Massive occurrence of the heterokont and fungal parasites Anisolpidium, Eury-chasma and Chytridium in Pylaiella littoralis (Ectocarpales, Phaeophyceae). Nova Hedwigia 69: 381-389
Küpper FC, Maier I, Müller DG, Loiseaux-de Goër S, Guillou L (2006) Phylogenetic affinities of two eukaryotic pathogens of marine macroalgae, Eurychasma dicksonii (Wright) Magnus and Chytridium polysiphoniae Cohn. Cryptogam Algol 27: 165-184
Macey BM, Christison KW, Mouton A (2011) Halioticida noduliformans isolated from cultured abalone (Haliotis midae) in South Africa. Aquaculture 315: 187-195
Marano AV, Pires-Zottarelli CLA, de Souza JI, Glockling SL and others (2012) Hyphochytriomycota, Oomycota and Perkinsozoa (supergroup Chromalveolata). In: Jones EBG, Pang KL (eds) Marine fungi and fungal-like organisms. de Gruyter, Berlin, p 167-214
McKone KL, Tanner CE (2009) Role of salinity in the susceptibility of eelgrass Zostera marina to the wasting disease pathogen Labyrinthula zosterae. Mar Ecol Prog Ser 377: 123-130
Müller DG, Küpper FC, Küpper H (1999) Infection experiments reveal broad host ranges of Eurychasma dicksonii (Oomycota) and Chytridium polysiphoniae (Chytridi o-my cota), two eukaryotic parasites of marine brown algae (Phaeophyceae). Phycological Res 47: 217-223
Muraosa Y, Morimoto K, Sano A, Nishimura K, Hatai K (2009) A new peronosporomycete, Halioticida noduliformans gen. et sp. nov., isolated from white nodules in the abalone Haliotis spp. from Japan. Mycoscience 50: 106-115
Park MG, Yih W, Coats DW (2004) Parasites and phytoplankton, with special emphasis on dinoflagellate infections. J Eukaryot Microbiol 51: 145-155
Parlakay A, Sukatar A, Senkardesler A (2005) Marine flora between south Ce me and Cape Teke (Izmir, Aegean Sea, Turkey). EU J Fish Aquat Sci 22: 187-194
Petersen AB, Rosendahl S (2000) Phylogeny of the Pero no-sporomycetes (Oomycota) based on partial se quen ces of the large ribosomal subunit (LSU rDNA). Mycol Res 104: 1295-1303
Petersen HE (1905) Contributions à la connaisance des phycomycètes marins (Chytridinae Fischer). K Dan Vidensk Selsk Forh 5: 439-488
Riisberg I, Orr RJS, Kluge R, Shalchian-Tabrizi K and others (2009) Seven gene phylogeny of heterokonts. Protist 160: 191-204
Robideau GP, De Cock AWAM, Coffey MD, Voglmayr H and others (2011) DNA barcoding of oomycetes with cytochrome c oxidase subunit I and internal transcribed spacer. Mol Ecol Resour 11: 1002-1011
Ruiz GM, Rawlings TK, Dobbs FC, Drake LA, Mullady T, Huq A, Colwell RR (2000) Global spread of microorganisms by ships. Nature 408: 49-50
Sekimoto S, Hatai K, Honda D (2007) Molecular phylogeny of an unidentified Haliphthoros-like marine oomycete and Haliphthoros milfordensis inferred from nuclearencoded small- and large-subunit rRNA genes and mitochondrial-encoded cox2 gene. Mycoscience 48: 212-221
Sekimoto S, Beakes GW, Gachon CMM, Müller DG, Küpper FC, Honda D (2008) The development, ultrastructural cytology, and molecular phylogeny of the basal oomy-cete Eurychasma dicksonii, infecting the filamentous phaeophyte algae Ectocarpus siliculosus and Pylaiella littoralis. Protist 159: 299-318
Sekimoto S, Klochkova TA, West JA, Beakes GW, Honda D (2009) Olpidiopsis bostrychiae sp. nov.: an endoparasitic oomycete that infects Bostrychia and other red algae (Rhodophyta). Phycologia 48: 460-472
Sime-Ngando T, Lefèvre E, Gleason F (2011) Hidden diversity among aquatic heterotrophic flagellates: ecological potentials of zoosporic fungi. Hydrobiologia 659: 5-22
Sparrow FK (1960) Aquatic phycomycetes, 2nd edn. The University of Michigan Press, Ann Arbor, MI
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690
Streftaris N, Zenetos A (2006) Alien marine species in the Mediterranean-the 100 'worst invasives' and their impact. Mediterr Mar Sci 7: 87-118
Strittmatter M, Gachon CMM, Küpper FC (2009) Ecology of lower oomycetes. In: Lamour KH, Kamoun S (eds) Oomycete genetics and genomics: diversity, interactions and research tools. John Wiley & Sons, Hoboken, NJ, p 25-46
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56: 564-577
Taskin E, Ozturk M (2007) The marine brown algae of the east Aegean Sea and Dardanelles. I. Ectocarpaceae, Pylaiellaceae, Chordariaceae, Elachistaceae and Giraudiaceae. Cryptogam Algol 28: 169-190
Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421: 628-630
Tsiamis K, Verlaque M, Panayotidis P, Montesanto B (2010) New macroalgal records for the Aegean Sea (Greece, eastern Mediterranean Sea). Bot Mar 53: 319-331
Tsiamis K, Panayotidis P, Economou-Amilli A, Katsaros C (2013a) Seaweeds of the Greek coasts. I. Phaeophyceae. Mediterr Mar Sci 14:141-157
Tsiamis K, Panayotidis P, Salomidi M, Pavlidou A, Kleinteich J, Balanika K, Küpper FC (2013b) Macroalgal community response to re-oligotrophication in Saronikos Gulf. Mar Ecol Prog Ser 472: 73-85
Van der Auwera G, Chapelle S, De Wachter R (1994) Structure of the large ribosomal subunit RNA of Phytophthora megasperma, and phylogeny of the oomycetes. FEBS Lett 338: 133-136
Van der Auwera G, De Baere R, Van de Peer Y, De Rijk P, Van den Broeck I, De Wachter R (1995) The phylogeny of the Hyphochytriomycota as deduced from ribosomal RNA sequences of Hyphochytrium catenoides. Mol Biol Evol 12: 671-678
West JA, Klochkova TA, Kim GH, Loiseaux-de Goer S (2006) Olpidiopsis sp., an oomycete from Madagascar that infects Bostrychia and other red algae: host species susceptibility. Phycological Res 54: 72-85
Wilce RT, Schneider CW, Quinlan AV, van den Bosch K (1982) The life history and morphology of free-living Pilayella littoralis (l.) Kjellman (Ectocarpaceae, Ectocarpales) in Nahant Bay, Massachusetts. Phycologia 21: 336-354