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Parasitic Chytrids: Their Effects on Phytoplankton Communities and Food-Web Dynamics

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Parasitic Chytrids: Their Effects on Phytoplankton Communities and Food-Web Dynamics View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Springer - Publisher Connector Hydrobiologia (2007) 578:113–129 DOI 10.1007/s10750-006-0438-z PHYTOPLANKTON WORKSHOP Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics Maiko Kagami Æ Arnout de Bruin Æ Bas W. Ibelings Æ Ellen Van Donk Ó Springer Science+Business Media B.V. 2007 Abstract Many phytoplankton species are suscep- selected on the basis of size is not clear. The tible to fungal parasitism. Parasitic fungi of phyto- dynamics of chytrids epidemics in a number of plankton mainly belong to the Chytridiomycetes studies were partly explained by environmental (chytrids). Here, we discuss the progression made in factors such as light, temperature, nutrients, pH, the study of chytrids that parasitize phytoplankton turbulence and zooplankton grazing. No general- species. Specific fluorescent stains aid in the iden- ization was made about the epidemic conditions; tification of chytrids in the field. The established some state unfavorable conditions for the host culturing methods and the advances in molecular growth support epidemic development, while others science offer good potential to gain a better insight report epidemics even under optimal growth into the mechanisms of epidemic development of conditions for the host. Phytoplankton is not chytrids and coevolution between chytrids and their defenseless, and several mechanisms have been algal hosts. Chytrids are often considered to be suggested, such as a hypersensitivity response, highly host-specific parasites, but the extent of host chemical defense, maintaining a high genetic diver- specificity has not been fully investigated. Chytrids sity and multitrophic indirect defenses. Chytrids may prefer larger host cells, since they would gain may also play an important role in food webs, more resources, but whether hosts are really because zoospores of chytrids have been found to be a good food source for zooplankton. Guest editors: M. Albay, J. Padisa´k & L. Naselli-Flores Morphological plasticity of phytoplankton under different Keywords Host–parasite interactions Á environmental constraints. Epidemics Á Host specificity Á Cell size Á Defense Á Food webs M. Kagami Á A. de Bruin Á B. W. Ibelings Á E. Van Donk Department of Food Web Studies, Center for Limnology, Netherlands Institute of Ecology Introduction (NIOO-KNAW), Rijksstraatweg 6, 3631AC Nieuwersluis, The Netherlands Fungal parasitism on phytoplankton is still a Present Address: neglected subject, although progress has been made M. Kagami (&) during the last decades. We are not the first to make Department of Environmental Science, Faculty of this observation (see e.g. Cook, 1963; Masters, 1976; Science, Toho University, Miyama 2-2-1, Funabashi 274-8510, Japan Reynolds, 1984; Van Donk & Bruning, 1992). This e-mail: [email protected] neglect is partly a consequence of the nature of 123 114 Hydrobiologia (2007) 578:113–129 parasitic infections: they often escape the notice of where recent updates of chytrids taxonomy can be non-specialists, and their epidemic development is found. often unpredictable, which has made it difficult to study chytrids in relation to other factors affecting phytoplankton populations (Reynolds, 1984; Van Visualization of chytrids Donk, 1989). On the other hand, Bruning (1991c) emphasized that fungal parasitism, unlike graz- Chytrids may remain undetected by non-special- ing or sedimentation, is a loss factor which is ists or are often confused with other organisms, for directly perceptible. This should facilitate field instance flagellates such as Bicosoeca (Canter investigations, especially when specific fluorescent Lund & Lund, 1995). These flagellate protozoans stains—which avoid confusion with other attached feed on bacteria, and do not harm the algae to non-parasitic organisms—are used (Mu¨ller & which they are attached. Special dyes and key Sengbusch, 1983). In addition, established culture morphological differences are helpful to identify systems make experimental work possible, which and distinguish chytrids from other organisms with should help to unravel the mechanisms underlying a chytrid-like appearance. Zoospores of chytrids epidemic development. have a single straight flagellum (Canter, 1967), and The work devoted to taxonomy and occurrence a spherical body (2–3 lm in diameter) containing a of algal parasites by a relatively small number of conspicuous oil globule and a single nucleus. This researchers in the 1940s, 1950s and 1960s (Ingold, oil globule is already quite visible (at a magnifica- 1940, 1941, 1944; Canter, 1946, 1947a, b, c; Canter tion of 400·), but can also be stained with Nile Red & Lund, 1948; Canter, 1949a, b, c, 1950a, b, c, (Kudoh, 1990). The nucleus can be stained with 1951; Canter & Lund, 1951; Canter, 1953; Canter 4¢,6-diamidino-2-phenilindole (DAPI) or Syber & Lund, 1953; Canter, 1954, 1960, 1961, 1966, green (Noble & Fuhrman, 1998). Before staining, 1967, 1968, 1969; Canter & Lund, 1969) may give the samples should be fixed with glutaraldehyde the impression that ‘‘fungal parasites have been (1% final concentration). Therefore, 1-mL sam- studied for a considerable period of time, and ples are put into Utermohl counting chambers, to indeed much has been learned about the occur- which 100 lgL–1 of Nile Red and 50 lgL–1 of rence of chytrids from these works. 4¢,6-diamidino-2-phenilindole (DAPI) were added Molecular science has progressed a great deal (both in final concentrations). The samples are since the 1960s. Molecular studies now firmly then incubated for 30 min in the dark at room place the Chytridiomycetes within the fungal temperature. Nile Red stains the oil globule kingdom (Bowman et al., 1992; Tehler et al., of the zoospores, emitting a characteristic 2000). The progress of molecular techniques and orange fluorescence under green excitation the well established cultural system offer us new (525 nm). DAPI stains the nucleus emitting blue possibilities to study chytrid dynamics with a fluorescence under ultraviolet (UV) excitation higher resolution than before, and to challenge (365 nm). some research questions that have not yet been Chytrids in the different stages of their life cycle solved. Intriguing questions include coevolution (attached zoospores, sporangia and empty sporan- between phytoplankton and chytrids, or the role gia) can be stained with CalcoFluor White (Mu¨ller of chytrids in the food-web dynamics. In this & Sengbusch, 1983). Three drops of 10% KOH paper, we give a general description of chytrids solution and three drops of 0.1% CalcoFluor White with relatively detailed attention to methods used solution were added to 1-mL samples in Utermohl in the study of chytrids, and a special emphasis on counting chambers, after which the samples were more recent developments in this research. This incubated for 10 min. CalcoFluor White binds to paper complements and builds on information chitin, a cell wall component of chytrids. The summarized in an earlier review (Ibelings et al., sample should be fresh or fixed with gultaralde- 2004). We refer the taxonomy and life cycle of hyde, but not with Lugol’s solution. A more chytrids to Ibelings et al. (2004), and to Chytrid detailed protocol can be obtained at Mycology Fungi Online: (http://www.bama.ua.edu/~nsfpeet) online (http://www.mycology.adelaide.edu.au/). 123 Hydrobiologia (2007) 578:113–129 115 Culturing chytrids ever, need special attention that bacteria should not outgrow the chytrids. With some effort parasitic chytrids can be isolated from lakes using elongated micropipettes and an inverted microscope and maintained in the labo- Parameters for fungal infection ratory. The isolated infected host cells are trans- ferred into fresh uninfected host cultures, which The most common parameter quantifying the then are kept under favorable environmental impact of chytrids on their host populations is the conditions for growth of the chytrids (relatively so-called prevalence of infection (proportion of high light and temperature, see Bruning, 1991b). infected cells, the percentages of infected cells) This way, parasite cultures are obtained as a non- (Bruning et al., 1992; Holfeld, 2000a). This axenic batch culture (Canter & Jaworski, 1978; parameter is calculated by dividing the number Bruning, 1991d). Freshly isolated infected host of infected cells by the total number of host cells, cells can also be used for the short-term exper- and is often expressed as the percentages of iments without maintaining in the laboratory infected cells. However, the prevalence of infec- (Van Donk & Ringelberg, 1983; Kagami & tion is not always the best parameter to quantify Urabe, 2002). the severity of fungal attacks. The chytrid, Zygorhizidium planktonicum can Another parameter to investigate the severity be maintained on its host algae, Asterionella of fungal epidemics is the mean intensity of formosa, in non-axenic batch cultures, using the infection, which is a quantification of the mean following procedure: 150-mL 1-week-old unin- number of fungi (attached zoospores and sporan- fected A. formosa host culture can be infected gia) per host cell in a population. This parameter with 5 to 10-mL of a 1-week-old Z. planktonicum is calculated by dividing the total number of fungi culture. The A. formosa host cultures can be attached to algal cells by the total number of host maintained on a modified Chu-10 medium (Stein, cells (Holfeld, 2000a). This parameter normalizes 1973) at 40 lmol quanta m–2 s–1 with a 14:10 h the host cell density, and expresses how many light :dark cycle and a temperature of 18°C. fungi succeed in attachment to their host. Multi- Culture conditions should be modified according ple infections (more than one parasite per host to the particular growth rates of chytrids and host cell) can be expressed only by the mean intensity algae (Bruning, 1991b). of infection. Multiple infections can have a large Highly infected host cultures are characterized impact on host death rate, and to take this into by multiple infected cells and free-swimming account mean intensity of infection is more zoospores in the medium.
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