Phytoplankton chytridiomycosis: community structure and infectivity of fungal parasites in aquatic ecosystems

Fungal parasitism is recurrent in plankton communities, especially in the form of parasitic chytrids. However, few attempts have been made to study the community structure and activity of parasites at the natural community level. To analyse the dynamics of zoosporic fungal parasites (i.e. chytrids) of phytoplankton, samples were collected from February to December 2007 in two freshwater lakes. Infective chytrids were omnipresent in lakes, with higher diversity of parasites and infected phytoplankton than in previous studies. The abundance and biomass of parasites were significantly higher in the productive Lake Aydat than in the oligomesotrophic Lake Pavin, while the infection prevalence in both lakes were similar and averaged about 20%. The host species composition and their size appeared as critical for chytrid infectivity, the larger hosts being more vulnerable, including pennate diatoms and desmids in both lakes. The highest prevalence (98%) was noted for the autumn bloom of the cyanobacterium Anabaena flosaquae facing the parasite Rhizosiphon crassum in Lake Aydat. Because parasites killed their hosts, this implies that cyanobacterial blooms, and other large size inedible phytoplankton blooms as well, may not totally represent trophic bottlenecks because their zoosporic parasites can release dissolved substrates for microbial processes through host destruction, and provide energetic particles as zoospores for grazers. Overall, we conclude that the parasitism by zoosporic fungi represents an important ecological driving force in the food web dynamics of aquatic ecosystems, and infer general empirical models on chytrid seasonality and trophodynamics in lakes.     

Comparison of sterol and fatty acid profiles of chytrids and their hosts reveals trophic upgrading of nutritionally inadequate phytoplankton by fungal parasites

Chytrids are ubiquitous fungal parasites in aquatic ecosystems, infecting representatives of all major phytoplankton groups. They repack carbon from inedible phytoplankton hosts into easily ingested chytrid propagules (zoospores), rendering this carbon accessible to zooplankton. Grazing on zoospores may circumvent bottlenecks in carbon transfer imposed by the dominance of inedible or poorly nutritious phytoplankton (mycoloop). We explored qualitative aspects of the mycoloop by analysing lipid profiles (fatty acids, sterols) of two chytrids infecting two major bloom-forming phytoplankton taxa of contrasting nutritional value: the diatom Asterionella formosa and the filamentous cyanobacterium Planktothrix agardhii. The polyunsaturated fatty acid composition of chytrids largely reflected that of their hosts, highlighting their role as conveyors of otherwise inaccessible essential lipids to higher trophic levels. We also showed that chytrids are capable of synthesizing sterols, thus providing a source of these essential nutrients for grazers even when sterols are absent in their phytoplankton hosts. Our findings reveal novel qualitative facets of the mycoloop, showing that parasitic chytrids, in addition to making carbon and essential lipids available from inedible sources, also upgrade their host's biochemical composition by producing sterols de novo, thereby enhancing carbon and energy fluxes in aquatic food webs.     

The ecology of chytrids in aquatic ecosystems: roles in food web dynamics

Chytrids are very important components of freshwater ecosystems, but the ecological significance of this group of fungi is not well understood. This review considers some of the significant environmental factors affecting growth and population composition of chytrids in aquatic habitats. The physical factors include primarily salinity, dissolved oxygen concentration and temperature. The biological factors include the role of chytrids as saprobes and parasites and methods of dispersal of propagules throughout the ecosystem. Dispersal depends upon both zoospores for short range and whole thalli for long range dispersal. Five roles for chytrids in food-web dynamics are proposed: (1) chytrid zoospores are a good food source for zooplankton, (2) chytrids decompose particulate organic matter, (3) chytrids are parasites of aquatic plants, (4) chytrids are parasites of aquatic animals and (5) chytrids convert inorganic compounds into organic compounds. New molecular methods for analysis of chytrid diversity in aquatic environments have the potential to provide accurate quantitative data necessary for better understanding of ecological processes in aquatic ecosystems.     

Parasitic chytrids could promote copepod survival by mediating material transfer from inedible diatoms

Diatoms form large spring blooms in lakes and oceans, providing fuel for higher trophic levels at the start of the growing season. Some of the diatom blooms, however, are not grazed by filter-feeding zooplankton like Daphnia due to their large size. Several of these large diatoms are susceptible to chytrid infections. Zoospores of chytrids appeared to be excellent food for Daphnia, both in terms of size, shape, and quality (PUFAs and cholesterol). Thus, zoospores of chytrids can bridge the gap between inedible diatoms and Daphnia. In order to examine the effects of diatoms and chytrids on the survival of copepods, we performed one grazing and one survival experiment. The grazing experiment revealed that the diatom, Asterionella formosa, was not grazed by the copepod, Eudiaptomus gracilis, even after being infected by the chytrid Zygorhizidium planktonicum. However, carbon and nitrogen concentrations were significantly reduced by E. gracilis only when A. formosa was infected by Z. planktonicum, indicating that the chytrids might facilitate material transfer from inedible diatoms to the copepods. The survival experiment revealed that E. gracilis lived shorter with A. formosa than with the cryptophyta Cryptomonas pyrenoidifera. However, the survival of E. gracilis increased significantly in the treatment where A. formosa cells were infected by Z. planktonicum. Since E. gracilis could not graze A. formosa cells due to their large colonial forms, E. gracilis may acquire nutrients by grazing on the zoospores, and were so able to survive in the presence of the A. formosa. This provides new insights into the role of parasitic fungi in aquatic food webs, where chytrids may improve copepod survival during diatom blooms.     

Functional effects of parasites on food web properties during the spring diatom bloom in Lake Pavin: a linear inverse modeling analysis

This study is the first assessment of the quantitative impact of parasitic chytrids on a planktonic food web. We used a carbon-based food web model of Lake Pavin (Massif Central, France) to investigate the effects of chytrids during the spring diatom bloom by developing models with and without chytrids. Linear inverse modelling procedures were employed to estimate undetermined flows in the lake. The Monte Carlo Markov chain linear inverse modelling procedure provided estimates of the ranges of model-derived fluxes. Model results support recent theories on the probable impact of parasites on food web function. In the lake, during spring, when 'inedible' algae (unexploited by planktonic herbivores) were the dominant primary producers, the epidemic growth of chytrids significantly reduced the sedimentation loss of algal carbon to the detritus pool through the production of grazer-exploitable zoospores. We also review some theories about the potential influence of parasites on ecological network properties and argue that parasitism contributes to longer carbon path lengths, higher levels of activity and specialization, and lower recycling. Considering the "structural asymmetry" hypothesis as a stabilizing pattern, chytrids should contribute to the stability of aquatic food webs.     

Community Structure of Planktonic Fungi and the Impact of Parasitic Chytrids on Phytoplankton in Lake Inba,Japan

Freshwater fungi have received little attention by scientific research in recent years, especially fungi of the pelagic zone. Recently, parasitic fungi, termed chytrids, have been found to play important roles in aquatic food webs. Yet, the diversity and community structure of planktonic fungi including chytrids are not well studied. In this study, we examined the temporal fluctuations of freshwater fungi, including chytrids, in Lake Inba by using molecular techniques of denaturing gradient gel electrophoresis (DGGE). DGGE profiles, and associated sequence analysis, indicated that chytrids were present on all sampling dates from May to October (n = 12). In addition, analysis showed that a large proportion of the sequences belonged to chytrids of both parasitic and saprotrophic species. This finding was supported by microscopic observations using Calcofluor white to stain chytrids infecting various phytoplankton species. The percentages of infection by chytrids on two dominant diatom species, Aulacoseira granulata and Aulacoseira ambigua, showed a similar seasonal pattern in the DGGE band profiles. From the phylogenetic analysis and microscopic identification, the chytrids infecting the two diatoms are likely to be affiliated to Chytriomyces sp. and Zygorhizidium sp.. This is the first study to show that DGGE is a useful preliminary approach for examining the diversity of planktonic fungi including chytrids. Our results indicate both parasitic and saprotrophic chytrids are a significant component of freshwater fungi inhabiting the pelagic zone of Lake Inba, Japan. Further modification of DGGE, together with new molecular techniques and microscopic observation, would reveal the hidden diversity and ecological significance of planktonic fungi in aquatic ecosystems.     

Roles of parasitic fungi in aquatic food webs: a theoretical approach

1. Parasites are ubiquitous in ecosystems, but their roles in material transfer are poorly understood. Fungal parasites in freshwater ecosystems are of major importance to small heterotrophic eukaryotes and consume large phytoplankton that are resistant to zooplankton grazing. 2. To evaluate their ecosystem‐level effects, we developed a simple food web model that incorporates competition between small and large phytoplankton for nutrients, zooplankton grazing on small phytoplankton, fungal parasitism on large phytoplankton and includes a newly discovered trophic link from fungal zoospores to zooplankton (F‐Z link). 3. Our model demonstrates the likely occurrence of an indirect mutualism between fungi and zooplankton, in which fungal parasitism increases zooplankton production by reducing the biomass of inedible large phytoplankton. Contradicting the expectation from a previous short‐term experiment that the F‐Z link may benefit zooplankton, the presence of the F‐Z link can reduce material transfer from phytoplankton to zooplankton because of the negative effect of the indirect mutualism. The model indicates that high growth efficiency of fungi on host tissue and their high nutrient status for zooplankton are crucial for the F‐Z link to increase zooplankton production. 4. The model also indicates that the contribution of material transfer via F‐Z link to zooplankton increases with nutrient availability. Our results suggest that parasitic fungi may be a key player in material transfer, especially in eutrophic ecosystems.     

Development of a Real-Time PCR assay for quantitative assessment of uncultured freshwater zoosporic fungi

Recently, molecular environmental surveys of the eukaryotic microbial community in lakes have revealed a high diversity of sequences belonging to uncultured zoosporic fungi. Although they are known as saprobes and algal parasites in freshwater systems, zoosporic fungi have been neglected in microbial food web studies. Recently, it has been suggested that zoosporic fungi, via the consumption of their zoospores by zooplankters, could transfer energy from large inedible algae and particulate organic material to higher trophic levels. However, because of their small size and their lack of distinctive morphological features, traditional microscopy does not allow the detection of fungal zoospores in the field. Hence, quantitative data on fungal zoospores in natural environments is missing. We have developed a quantitative PCR (qPCR) assay for the quantification of fungal zoospores in lakes. Specific primers were designed and qPCR conditions were optimized using a range of target and non-target plasmids obtained from previous freshwater environmental 18S rDNA surveys. When optimal DNA extraction protocol and qPCR conditions were applied, the qPCR assay developed in this study demonstrated high specificity and sensitivity, with as low as 100 18S rDNA copies per reaction detected. Although the present work focuses on the design and optimization of a new qPCR assay, its application to natural samples indicated that qPCR offers a promising tool for quantitative assessment of fungal zoospores in natural environments. We conclude that this will contribute to a better understanding of the ecological significance of zoosporic fungi in microbial food webs of pelagic ecosystems.     

Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics

Many phytoplankton species are susceptible to fungal parasitism. Parasitic fungi of phytoplankton mainly belong to the Chytridiomycetes (chytrids). Here, we discuss the progression made in the study of chytrids that parasitize phytoplankton species. Specific fluorescent stains aid in the identification of chytrids in the field. The established culturing methods and the advances in molecular science offer good potential to gain a better insight into the mechanisms of epidemic development of chytrids and coevolution between chytrids and their algal hosts. Chytrids are often considered to be highly host-specific parasites, but the extent of host specificity has not been fully investigated. Chytrids may prefer larger host cells, since they would gain more resources, but whether hosts are really selected on the basis of size is not clear. The dynamics of chytrids epidemics in a number of studies were partly explained by environmental factors such as light, temperature, nutrients, pH, turbulence and zooplankton grazing. No generalization was made about the epidemic conditions; some state unfavorable conditions for the host growth support epidemic development, while others report epidemics even under optimal growth conditions for the host. Phytoplankton is not defenseless, and several mechanisms have been suggested, such as a hypersensitivity response, chemical defense, maintaining a high genetic diversity and multitrophic indirect defenses. Chytrids may also play an important role in food webs, because zoospores of chytrids have been found to be a good food source for zooplankton.     

Food quantity and quality regulation of trophic transfer between primary producers and a keystone grazer (Daphnia) in pelagic freshwater food webs

The transfer of energy and nutrients from plants to animals is a key process in all ecosystems. In lakes, inefficient transfer of primary producer derived energy can result in low animal growth rates, accumulation of nuisance phytoplankton blooms and dissipation of energy from the ecosystem. Most research on carbon transfer efficiency in pelagic food webs has focused on either food quantity or food quality, with the latter considered separately as either elemental stoichiometry or biochemical composition. The natural occurrence and magnitude of these types of growth limitations and their combined effects on Daphnia , a keystone grazer in pelagic freshwater ecosystems, are largely unknown. Our empirical models predict that the strength and nature of food quantity and quality limitation varies greatly with lake trophic state (total phosphorus, TP) and that Daphnia growth rates and thus energy and nutrient transfer efficiency are highest in lakes with intermediate trophic status (TP 10–25 μg l⁻¹). We predict that food availability place the greatest constraint on Daphnia growth in nutrient poor lakes (TP≤4 μg l⁻¹). Phosphorus limitation of Daphnia growth increased with decreasing TP, but the overall effect was never predicted to be the dominant constraining factor. Eicosapentaenoic acid (EPA, 20:5ω3) limitation was predicted to occur in both nutrient poor and nutrient rich lakes and placed the primary constraint on food quality in the most productive lakes. Two contrasting EPA-models gave different results on the magnitude of EPA-limitation, implying that additional food quality factors decrease Daphnia growth at high TP. In conclusion, the model predicts that Daphnia growth should peak in mesotrophic lakes, food quantity will place the greatest constraint on growth in oligotrophic lakes and EPA will primarily limit growth in eutrophic lakes.     

Fluorescence in situ hybridization of uncultured zoosporic fungi: Testing with clone-FISH and application to freshwater samples using CARD-FISH

Recently, molecular environmental surveys of the eukaryotic microbial community in lakes have revealed a high diversity of sequences belonging to uncultured zoosporic fungi commonly known as chytrids. These microorganisms have two different stages in their life cycle and are known as algal parasites (i.e. host-attached infective sporangia) and as food sources for zooplankton (i.e. free-living zooflagellate propagules) in aquatic systems. However, because of their small size and their lack of distinctive morphological features, traditional microscopy does not allow the detection of chytrids, particularly of zoospores which have probably been misidentified as phagotrophic flagellates in previous studies. Hence, quantitative data on chytrids in natural environments is missing. We have adapted a clone-FISH approach known from prokaryotes to optimize the hybridization conditions of a designed oligonucleotidic probe specific to Chytridiales (i.e. the largest group of the true-fungal division of Chytridiomycota), before application to natural samples using the CARD-FISH approach. When these conditions were applied, the CARD-FISH assay demonstrated high specificity and sensitivity, and offers a promising tool for quantitative assessment of natural zoosporic fungi, primarily of zoospores which contributed up to 60% of the total abundance of heterotrophic flagellates. Although the field results from the CARD-FISH approach were considered preliminary and mainly as ‘proof of concept’, findings were consistent with ecological considerations known from pelagic habitats and host versus parasite populations, with recurrent ecological patterns in two contrasting lake ecosystems. We conclude that this approach will contribute to a better understanding of the ecological significance of zoosporic organisms in microbial food webs of pelagic ecosystems.     

Warming accelerates termination of a phytoplankton spring bloom by fungal parasites

Climate change is expected to favour infectious diseases across ecosystems worldwide. In freshwater and marine environments, parasites play a crucial role in controlling plankton population dynamics. Infection of phytoplankton populations will cause a transfer of carbon and nutrients into parasites, which may change the type of food available for higher trophic levels. Some phytoplankton species are inedible to zooplankton, and the termination of their population by parasites may liberate otherwise unavailable carbon and nutrients. Phytoplankton spring blooms often consist of large diatoms inedible for zooplankton, but the zoospores of their fungal parasites may serve as a food source for this higher trophic level. Here, we investigated the impact of warming on the fungal infection of a natural phytoplankton spring bloom and followed the response of a zooplankton community. Experiments were performed in ca. 1000 L indoor mesocosms exposed to a controlled seasonal temperature cycle and a warm (+4 °C) treatment in the period from March to June 2014. The spring bloom was dominated by the diatom Synedra. At the peak of infection over 40% of the Synedra population was infected by a fungal parasite (i.e. a chytrid) in both treatments. Warming did not affect the onset of the Synedra bloom, but accelerated its termination. Peak population density of Synedra tended to be lower in the warm treatments. Furthermore, Synedra carbon: phosphorus stoichiometry increased during the bloom, particularly in the control treatments. This indicates enhanced phosphorus limitation in the control treatments, which may have constrained chytrid development. Timing of the rotifer Keratella advanced in the warm treatments and closely followed chytrid infections. The chytrids' zoospores may thus have served as an alternative food source to Keratella. Our study thus emphasizes the importance of incorporating not only nutrient limitation and grazing, but also parasitism in understanding the response of plankton communities towards global warming.     

Unveiling fungal zooflagellates as members of freshwater picoeukaryotes: evidence from a molecular diversity study in a deep meromictic lake

This study presents an original 18S rRNA PCR survey of the freshwater picoeukaryote community, and was designed to detect unidentified heterotrophic picoflagellates (size range 0.6-5 microm) which are prevalent throughout the year within the heterotrophic flagellate assemblage in Lake Pavin. Four clone libraries were constructed from samples collected in two contrasting zones in the lake. Computerized statistic tools have suggested that sequence retrieval was representative of the in situ picoplankton diversity. The two sampling zones exhibited similar diversity patterns but shared only about 5% of the operational taxonomic units (OTUs). Phylogenetic analysis clustered our sequences into three taxonomic groups: Alveolates (30% of OTUs), Fungi (23%) and Cercozoa (19%). Fungi thus substantially contributed to the detected diversity, as was additionally supported by direct microscopic observations of fungal zoospores and sporangia. A large fraction of the sequences belonged to parasites, including Alveolate sequences affiliated to the genus Perkinsus known as zooparasites, and chytrids that include host-specific parasitic fungi of various freshwater phytoplankton species, primarily diatoms. Phylogenetic analysis revealed five novel clades that probably include typical freshwater environmental sequences. Overall, from the unsuspected fungal diversity unveiled, we think that fungal zooflagellates have been misidentified as phagotrophic nanoflagellates in previous studies. This is in agreement with a recent experimental demonstration that zoospore-producing fungi and parasitic activity may play an important role in aquatic food webs.     

Prevalence of chytrid parasitism among diatom populations in the lower Columbia River (2009–2013)

相似文献   

The use of nutrient reduction and food-web management to improve water quality in the deep stratifying Wupper Reservoir, Germany

Only a combination of nutrient load abatement and food-web management proved efficient for the management of water quality in the deep stratifying Wupper Reservoir. Reduction of nutrient loading, was completed in winter 1992/1993, but resulted only in reduced winter/spring mixing of phosphorus concentrations. Since the capacity of the diatom spring bloom to remove nutrients from the trophogenic layer of this slightly eutrophic water-body was never exhausted, the surplus of total phosphorus available to support summer algal growth remained unchanged. Thus, nutrient reduction alone did not improve the water quality, as expected. Subsequent replacement of the smaller Daphnia cucullata by the larger Daphnia galeata-hyalina complex that was attributable to successful food-web management did, however, result in a shift from a turbid to a clear water regime in 1999. Clearly, the zooplankton community, and therefore food-web structure, played an integral role in nutrient recycling and in the repartitioning of the phosphorus pool. As diatom settling and grazing became much more tightly linked with the appearance of the larger-bodied Daphnia galeata-hyalina complex, which exploits lower-level food resources as early as May, daphnids increasingly acted as a sink for phosphorus. This increased export fluxes out of the pelagic zone and leaves a smaller surplus of total phosphorus to support the accumulation of summer algae. Consequently, water transparency and total chlorophyll concentrations in summer improved with food-web restructuring, indicating real oligotrophication of Wupper Reservoir driven by internal feedbacks. Handling editor: S. I. Dodson     

Transfer efficiency of carbon,nutrients, and polyunsaturated fatty acids in planktonic food webs under different environmental conditions

The trophic transfer efficiency (TTE) is an important indicator of ecosystem functioning. However, TTE data from freshwater food webs are ambiguous due to differences in time scales and methods. We investigated the transfer of essential substances (carbon, nutrients, and polyunsaturated fatty acids) through plankton communities in 30 Polish lakes with different trophic status in the middle of summer. The results of our study revealed that different essential substances were transferred from phytoplankton to zooplankton with varying efficiencies. The average TTE of C, N, P, and the sum of ω‐3 PUFA were 6.55%, 9.82%, 15.82%, and 20.90%, respectively. Our results also show a large mismatch between the elemental and biochemical compositions of zooplankton and their food during the peak of the summer stagnation, which may further promote the accumulation of essential substances. There were also large differences in TTEs between trophic conditions, with the highest efficiencies in oligotrophic lakes and the lowest in dystrophic and eutrophic lakes. Therefore, our study indicates that disturbances like eutrophication and dystrophication similarly decrease the TTE of essential substances between phytoplankton and zooplankton in freshwater food webs.     

Food webs: a plea for parasites

Parasites have the capacity to regulate host populations and may be important determinants of community structure, yet they are usually neglected in studies of food webs. Parasites can provide much of the information on host biology, such as diet and migration, that is necessary to construct accurate webs. Because many parasites have complex life cycles that involve several different hosts, and often depend on trophic interactions for transmission, parasites provide complementary views of web structure and dynamics. Incorporation of parasites in food webs can substantially after baste web properties, Including connectance, chain length and proportions of top and basal species, and can allow the testing of specific hypotheses related to food-web dynamics.     

Carbon and nutrients of indigestible pollen are transferred to zooplankton by chytrid fungi

相似文献   

Phylogeny and biogeography of an uncultured clade of snow chytrids

Numerous studies have shown that snow can contain a diverse array of algae known as ‘snow algae’. Some reports also indicate that parasites of algae (e.g. chytrids) are also found in snow, but efforts to phylogenetically identify ‘snow chytrids’ have not been successful. We used culture‐independent molecular approaches to phylogenetically identify chytrids that are common in long‐lived snowpacks of Colorado and Europe. The most remarkable finding of the present study was the discovery of a new clade of chytrids that has representatives in snowpacks of Colorado and Switzerland and cold sites in Nepal and France, but no representatives from warmer ecosystems. This new clade (‘Snow Clade 1’ or SC1) is as deeply divergent as its sister clade, the Lobulomycetales, and phylotypes of SC1 show significant (P < 0.003) genetic‐isolation by geographic distance patterns, perhaps indicating a long evolutionary history in the cryosphere. In addition to SC1, other snow chytrids were phylogenetically shown to be in the order Rhizophydiales, a group with known algal parasites and saprotrophs. We suggest that these newly discovered snow chytrids are important components of snow ecosystems where they contribute to snow food‐web dynamics and the release of nutrients due to their parasitic and saprotrophic activities.