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The Ecological Potentials of Phytomyxea (''Plasmodiophorids

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The Ecological Potentials of Phytomyxea (''Plasmodiophorids Hydrobiologia (2011) 659:23–35 DOI 10.1007/s10750-010-0508-0 DISREGARDED DIVERSITY AND ECOLOGICAL POTENTIALS Review/Opinion Paper The ecological potentials of Phytomyxea (‘‘plasmodiophorids’’) in aquatic food webs Sigrid Neuhauser • Martin Kirchmair • Frank H. Gleason Received: 17 May 2010 / Revised: 14 September 2010 / Accepted: 24 September 2010 / Published online: 20 October 2010 Ó The Author(s) 2010. This article is published with open access at Springerlink.com Abstract The Phytomyxea (‘‘plasmodiophorids’’) the parasites. Furthermore, significant amounts of including both Plasmodiophorida and Phagomyxida nutrients derived from the hosts, both primary is a monophyletic group of Eukaryotes composed of producers (plants and algae) and primary consumers obligate biotrophic parasites of green plants, brown (litter decomposers and plant parasites [Oomycetes]), algae, diatoms and stramenopiles commonly found in can enter the food web at different trophic levels in many freshwater, soil and marine environments. form of zoospores and resting spores. Large numbers However, most research on Phytomyxea has been of zoospores and resting spores are produced which restricted to plant pathogenic species with agricul- can be eaten by secondary and tertiary consumers, tural importance, thereby missing the huge ecological such as grazing zooplankton and metazoan filter- potential of this enigmatic group of parasites. Mem- feeders. Therefore, these microbes can act as energy- bers of the Phytomyxea can induce changes in rich nutrient resources which may significantly alter biomass in their hosts (e.g. hypertrophies of the host the trophic relationships in fresh water, soil and tissue) under suitable environmental conditions. marine habitats. Based on the presented data, Phy- Upon infection they alter the metabolism of their tomyxea can significantly contribute to the complex- hosts, consequently changing the metabolic status of ity and energy transfer within food webs. their host. This results in an altered chemical composition of the host tissue, which impacts the Keywords Aquatic ecosystems Á Food webs Á diversity of species which feed on the tissues of Biotrophic parasites Á Plasmodiophora Á the infected host and on the zoospores produced by Host–pathogen interaction Guest editors: T. Sime-Ngando & N. Niquil / Disregarded Introduction Microbial Diversity and Ecological Potentials in Aquatic Systems During the past decade an unexpectedly high diver- sity of microbial eukaryotes has been revealed in S. Neuhauser (&) Á M. Kirchmair Institute of Microbiology, Leopold Franzens-University many aquatic habitats (Moreira & Lo´pez-Garcı´a, Innsbruck, Technikerstr. 25, 6020 Innsbruck, Austria 2002; Gleason et al., 2008; Lefe`vre et al., 2008; e-mail: [email protected] Lopez-Garcia & Moreira, 2008; Sime-Ngando et al., 2010). Amongst these eukaryotes the heterotrophic F. H. Gleason School of Biological Sciences A12, University of Sydney, flagellates are thought to play key roles in aquatic Sydney, NSW 2006, Australia ecosystems as parasites and saprobes. Heterotrophic 123 24 Hydrobiologia (2011) 659:23–35 flagellates (HF) are defined as microbes with zoo- on soil-borne plant pathogens. We expect that the spores approximately less than or equal to 5 lmin underlying mechanisms of parasitism are similar in diameter and without chlorophyll (Sime-Ngando all aquatic, soil and marine habitats. et al., 2010). Their roles in food webs include recycling inorganic and organic nutrients, contribut- ing to the energy flow in food webs, trophic Classification upgrading and regulation of population size of their hosts (Sime-Ngando et al., 2010). The Phytomyxea are a monophyletic group of Eukary- Based on the morphology of both the primary and otes. During the past few years the common name secondary zoosporic stages, Phytomyxea can be ‘‘plasmodiophorids’’ as introduced by Braselton has included in the ecological concept of HF as proposed been used for this group (Braselton, 1995). The true by Sime-Ngando et al. (2010). However, phytomyxean taxonomic position of this group has been debated zoospores lack distinctive morphological features frequently since the publication of the original which would allow them to be easily identified within description of Plasmodiophora brassicae Woronin a pool of HF. In the studies by Lefe`vre et al. (2007, (reviewed by Neuhauser et al., 2010). Woronin (1878) 2008) the analysis of HF populations revealed a classified Pl. brassicae originally as a protist (sensu considerable number of zoospores belonging to sapro- Haeckel). Later the Phytomyxea were thought to bic or parasitic zoosporic true fungi (Chytridiomycota, belong to the Mastigomycota together with other Blastocladiomycota, etc.) and groups of parasitic zoosporic fungi and stramenopiles. Sparrow (1960) protists. Although no Phytomyxea were detected by included them in the aquatic phycomycetes. Currently Lefe`vre et al. (2008), we propose that these microbes they are considered to be members of the protist are frequently present in freshwater, soil and marine supergroup Rhizaria, because the affiliation of Phy- ecosystems. Recently evidence has suggested that the tomyxea to the Rhizaria has been indicated repeatedly Phytomyxea have been under-sampled in DNA-based by molecular studies (Cavalier-Smith, 1993; Bulman environmental screening studies in many ecosystems et al., 2001; Archibald & Keeling, 2004; Nikolaev because of negative primer bias (Neuhauser et al., et al., 2004; Bass et al., 2009). Throughout this article 2010). However, DNA sequences of some previously we will use zoological nomenclature for the higher unknown taxa of Phytomyxea have been identified taxonomic levels. Tentatively the Class Phytomyxea is in clone libraries from a saline meromictic lake placed within the Phylum Cercozoa and the Subphy- (Takishita et al., 2007a), and in sediment of a deep lum Endomyxa (Bass et al., 2009). Based on 18S sea methane cold steep (Takishita et al., 2007b). rDNA data the Class Phytomyxea comprises two Furthermore, a high diversity of known and unsampled orders: Plasmodiophorida, which are mainly parasites taxa has been detected in randomly collected soil of green plants and the Phagomyxida which are and fresh water samples using primers specific for parasites of diatoms and brown algae. Currently there Plasmodiophorida (Neuhauser et al., unpublished). are 41 known species belonging to twelve genera Collectively these studies support the view that this (Table 1). group of microbes has been previously under-sampled in many ecosystems. Furthermore it can be expected that Phytomyxea are widely distributed in many Life cycles aquatic ecosystems and play more important roles as biotrophs than previously thought. All known species of Phytomyxea are obligate The purposes of this article are (i) to describe the biotrophs. These microbes have complex life cycles distinctive features of Phytomyxea, (ii) to provide the with two free swimming zoosporic stages, two basis for considering them as members of the HF plasmodial stages that are linked to the host, a thin- group and (iii) to discuss some of their potential walled zoosporangial stage and thick-walled resting ecological roles in freshwater, soil and marine spores. In some species the resting spores aggregate ecosystems. The ecological potential will be illus- into cytosori which are the most prominent and trated using data available from the sparse literature important morphological characteristic. The form, on aquatic hosts and from the more detailed studies size and pigmentation of the resting spores and the 123 Hydrobiologia (2011) 659:23–35 Table 1 Phytomyxean species according to Karling (1968) including the species described more recently Terrestrial Fresh water Marine Green plants Ligniera verrucosa Maire & A. Tisson Ligniera isoetes Palm Plasmodiophora bicaudata Feldmann Ligniera junci (Schwartz) Maire & A. Tisson* Ligniera junci Plasmodiophora diplantherae (Ferd. & Winge) Ivimey Ligniera pilorum Fron. & Gaillat Membranosorus heterantherae Ostenf. & H.E. Cook Ligniera betae (Neˇmec) Karling Petersen Plasmodiophora halophilae Ferd. & Winge Ligniera hypogeae (Borzı´) Karling Sorodiscus callitrichis Lagerh. & Winge Plasmodiophora maritima Feldm.-Maz. Ligniera plantaginis (Neˇmec) Karling Sorosphaera veronicae Tetramyxa parasitica K. I. Goebel Plasmodiophora brassicae Woronin Spongospora nasturtii M. W. Dick Polymyxa graminis Ledingham Tetramyxa triglochinis Molliard Polymyxa betae Keskin Sorodiscus radicicolus Ivimey Cook Sorosphaera veronicae J. Schro¨t. Sorosphaera radicalis Ivimey Cook & Schwartz* Sorosphaera viticola Kirchm., Neuh. & L. Huber Spongospora subterranea (Wallr.) Lagerh. Spongospora campanulae (Ferd. & Winge) Ivimey Cook Spongospora cotulae Barrett Tetramyxa rhizophaga Lihnell Tetramyxa elaeagni Y. Yendo & K. Takase Oomycetes Octomyxa achlyae Couch, J. Leitn. & Whiffen* Octomyxa achlyae* Octomyxa brevilegniae Pend.* Octomyxa brevilegniae* Woronina polycystis Cornu* Sorodiscus cokeri Goldie-Sm.* Woronina pythii Goldie-Sm.* Woronina leptolegnia Karling* Woronina polycystis* Woronina pythii* Green algae Sorodiscus karlingii Ivimey Cook s. l. Woronina aggregata Zopf Woronina glomerata (Cornu) A. Fisch 123 25 26 Hydrobiologia (2011) 659:23–35 mode of cytosoral aggregation are used for species delimitation in Plasmodiophorida. These thick-walled resting spores have not been identified in the Phag- omyxida yet. But recently evidence indicates that two . Species marked morphologically different types of zoospores
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