Parasitic chytrids sustain zooplankton growth during inedible algal bloom

Rasconi, Séréna; Grami, Boutheina; Niquil, Nathalie; Jobard, MarlÃ ̈ne; Sime-Ngando, Télesphore

doi:10.3389/fmicb.2014.00229

Cited by 46 publications

(51 citation statements)

References 117 publications

(169 reference statements)

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“…If more than four zoospores were produced per sporangium, as seen in multiple previous laboratory and field studies (38)(39)(40), then this suggests either that zoospores must obtain additional carbon from other sources besides the host or that the zoospores contain less than 10.7 pg carbon per cell, resulting in a lower carbon transfer efficiency. However, during blooms of large, inedible phytoplankton in French lakes, parasitism by chytrids and the subsequent production of zoospores was estimated to shunt ϳ20% of the total primary production into a form edible to zooplankton (18). Additionally, models that included parasitic chytrids showed an increase in carbon transfer efficiency and higher grazing efficiency than in a system lacking parasitic chytrids (41).…”

Section: Discussionmentioning

confidence: 99%

“…Zoospores were not only detected upstream from BAT, in the river, but also downstream, in the estuary and its lateral bays, potentially providing a previously unknown source of labile carbon to support estuarine food webs. The input of zoospores to the river and estuary may not be a trivial food source, since it has been shown that zoospores contribute to the mesozooplankton diet and can constitute up to 50 to 57% of the microzooplankton diet in French lakes (18).…”

Section: Discussionmentioning

confidence: 99%

“…While the host-attached stage of the parasitic chytrid life cycle (i.e., the sporangium) can easily be visualized using nonspecific fluorescent staining techniques such as calcofluor white, which stains chitin (16), the rou-tine enumeration of free-swimming infective zoospores within mixed plankton assemblages is quite difficult due to their small size, nondescript appearance, and lack of chitin (15,17). The more specific technique of fluorescence in situ hybridization (FISH) has been successfully employed to quantify chytrid zoospores in the field because it combines visual recognition of the zoospore life stage with a molecular identification probe (9,18); however, the procedure can be time-consuming and, therefore, is not amenable to rapid analysis or high-throughput approaches.…”

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confidence: 99%

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Enumeration of Parasitic Chytrid Zoospores in the Columbia River via Quantitative PCR

Maier

Peterson

2016

Appl Environ Microbiol

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Through lethal infection, fungal parasites of phytoplankton ("chytrids") repackage organic material from the large, effectively inedible, colonial diatoms they infect into much smaller zoospores, which are easier for zooplankton to consume. However, their small size and lack of distinguishing morphological features render it difficult to distinguish zoospores from other small flagellates in mixed assemblages in the natural environment. In this study, we developed and tested a method to quantify chytrid zoospores in field studies using quantitative PCR (qPCR) targeting the internal transcribed spacer 2 (ITS2) region within the rRNA gene cluster. To achieve accurate quantification, the assay was designed to be highly specific for a parasite (Rhizophydium planktonicum) of the diatom Asterionella formosa; however, the approach is applicable to additional host-parasite systems. Parasitic zoospores were detected and quantified in the freshwater reaches of the lower Columbia River, as well as in the salt-influenced estuary and river plume. The coincidence between zoospore abundances and a prevalence of small zooplankton during blooms of large, colonial diatoms in the spring suggests that Columbia River zooplankton may be poised to benefit nutritionally from chytrid zoospores, thus providing a mechanism to retain organic carbon within the system and reduce losses to downstream export. We estimate that ϳ15% of the carbon biomass tied up in blooms of the dominant diatom species is transformed into zoospores through the parasitic shunt during spring. IMPORTANCEThe small size of the parasitic fungi that infect phytoplankton makes it difficult to identify and quantify them in natural systems. We developed and tested a method to quantify these organisms (chytrid zoospores) using a molecular technique that targets the internal transcribed spacer region within the rRNA gene cluster. Using this method, we quantified the abundance of the motile stage of a specific parasite in the freshwater and saltwater-influenced regions of the Columbia River in the U.S. Pacific Northwest. Parasitic chytrid zoospores were found to be present throughout the year and at higher abundances during the spring, when phytoplankton blooms occur. The presence of these organisms indicates not only that they may be responsible for the death of host phytoplankton cells but that they may also provide a readily available food source to small consumers (zooplankton) in the food web of the Columbia River. Z oosporic fungi (chytrids) are common parasites of phytoplankton in aquatic systems. Unlike most fungi, the infective stage is a free-swimming zoospore that seeks out a host, attaches to it, and from successful attachment grows a mature sporangium within which new zoospores develop (1). Laboratory studies have shown that chytrid parasites of phytoplankton can effectively repackage organic material from large, functionally inedible, colonial diatoms into zoospores, which are easier for zooplankton to consume (2-5). A major limitation for field investig...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Enumeration of Parasitic Chytrid Zoospores in the Columbia River via Quantitative PCR

Maier

Peterson

2016

Appl Environ Microbiol

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“…This peak has been shown to exhibit a variable intensity depending on the season and year: it is sharper in spring and early summer and has been shown to be related to algal blooms [50,51]. Diatom frustules were predominant at these depths for the five sampling campaigns and contributed to massive precipitation of silica in the lake.…”

Section: Mineral Phases In the Superficial Zone Of The Lake (0-30-m Dmentioning

confidence: 96%

Mineralogical Diversity in Lake Pavin: Connections with Water Column Chemistry and Biomineralization Processes

et al. 2016

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Abstract:As biominerals are good tracers of microbial interactions with the environment, they may provide signatures of microbial evolution and paleoenvironmental conditions. Since modern analogues of past environments help with defining proxies and biosignatures, we explored microbe mineral interactions in the water column of a maar lake, located in France: Lake Pavin. This lake is considered as a potential Precambrian ocean analogue, as it is ferruginous and meromictic, i.e., stratified with a superficial O 2 -rich layer (mixolimnion) and a deeper permanently anoxic layer (monimolimnion). We combined bulk chemical analyses of dissolved and particulate matter in combination with electron microscopy analyses of the particulate matter at different depths along the water column. The mineralogy changed along with water chemistry, and most of the minerals were intimately associated with microorganisms. Evolution of the redox conditions with depth leads to the successive precipitation of silica and carbonates, Mn-bearing, Fe-bearing and S-containing phases, with a predominance of phosphates in the monimolimnion. This scheme parallels the currently-assessed changes of microbial diversity with depth. The present results corroborate previous studies that suggested a strong influence of microbial activity on mineralogical diversity through extracellular and intracellular biomineralization. This paper reports detailed data on mineralogical profiles of the water column and encourages extended investigation of these processes.

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“…For example, in laboratory experiments, a diet of zoospores has been shown to improve the fitness and survival of the zooplankter Daphnia, compared to a diet of large colonial host diatoms (9). The potential importance of chytrids in aquatic food webs has been reviewed at length (3,(10)(11)(12)(13)(14)(15); however, understanding of the role that chytrid zoospores play in food web dynamics is limited by the lack of robust methods to quantify parasitic zoosporic fungi in water samples and in the guts of consumers.…”

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confidence: 99%

Evaluation of Daphnid Grazing on Microscopic Zoosporic Fungi by Using Comparative Threshold Cycle Quantitative PCR

Maier

Uchii

Peterson

et al. 2016

Appl Environ Microbiol

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Lethal parasitism of large phytoplankton by chytrids (microscopic zoosporic fungi) may play an important role in organic matter and nutrient cycling in aquatic environments by shunting carbon away from hosts and into much smaller zoospores, which are more readily consumed by zooplankton. This pathway provides a mechanism to more efficiently retain carbon within food webs and reduce export losses. However, challenges in accurate identification and quantification of chytrids have prevented a robust assessment of the relative importance of parasitism for carbon and energy flows within aquatic systems. The use of molecular techniques has greatly advanced our ability to detect small, nondescript microorganisms in aquatic environments in recent years, including chytrids. We used quantitative PCR (qPCR) to quantify the consumption of zoospores by Daphnia in laboratory experiments using a culture-based comparative threshold cycle (C T ) method. We successfully quantified the reduction of zoospores in water samples during Daphnia grazing and confirmed the presence of chytrid DNA inside the daphnid gut. We demonstrate that comparative C T qPCR is a robust and effective method to quantify zoospores and evaluate zoospore grazing by zooplankton and will aid in better understanding how chytrids contribute to organic matter cycling and trophic energy transfer within food webs. IMPORTANCEThe study of aquatic fungi is often complicated by the fact that they possess complex life cycles that include a variety of morphological forms. Studies that rely on morphological characteristics to quantify the abundances of all stages of the fungal life cycle face the challenge of correctly identifying and enumerating the nondescript zoospores. These zoospores, however, provide an important trophic link between large colonial phytoplankton and zooplankton: that is, once the carbon is liberated from phytoplankton into the parasitic zoospores, the latter are consumed by zooplankton and carbon is retained in the aquatic food web rather than exported from the system. This study provides a tool to quantify zoospores and evaluate the consumption of zoospores by zooplankton in order to further our understanding of their role in food web dynamics. Many zoosporic fungi in the division Chytridiomycota (chytrids) are parasitic on phytoplankton and cause host cell death with every successful infection (1-3). When they reach epidemic proportions, parasitic infections can lead to bloom decline and modulation of species succession (4-6). Furthermore, zoosporic fungi may play an important role in the cycling of nutrients and organic matter in aquatic food webs through the liberation of organic matter from large hosts, which are generally inaccessible to small zooplankton. (This pathway from large inedible algae to zooplankton via zoospores is called the "mycoloop" [see references 7 and 8].) Chytrid zoospores are rich in polyunsaturated fatty acids, making them nutritious food items for filter-feeding zooplankton. For example, in laboratory experiment...

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Parasitic chytrids sustain zooplankton growth during inedible algal bloom

Cited by 46 publications

References 117 publications

Enumeration of Parasitic Chytrid Zoospores in the Columbia River via Quantitative PCR

Enumeration of Parasitic Chytrid Zoospores in the Columbia River via Quantitative PCR

Mineralogical Diversity in Lake Pavin: Connections with Water Column Chemistry and Biomineralization Processes

Evaluation of Daphnid Grazing on Microscopic Zoosporic Fungi by Using Comparative Threshold Cycle Quantitative PCR

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