Short CommunicationFungicides at environmentally relevant concentrations can promote the proliferation of toxic bloom-forming cyanobacteria by inhibiting natural fungal parasite epidemics
Introduction
Cyanobacterial blooms raise serious public health concerns, as many cyanobacterial taxa produce diverse toxic metabolites with hepatotoxic, cytotoxic, neurotoxic or tumor promoting effects (Falconer, 2005, Araoz et al., 2010) that can accumulate along the food chain (Ibelings and Chorus, 2007). The management of cyanobacterial blooms has hence become an important priority for environmental agencies, water authorities and health organizations (Huisman et al., 2018). Extensive research has demonstrated that the intensity, frequency and toxicity of cyanobacterial blooms have increased over recent decades, chiefly due to over–supply of phosphorous and nitrogen as a result of anthropogenic eutrophication, together with global warming (Wagner and Adrian, 2009, Paerl and Otten, 2013). Yet, relatively sharper increases in cyanobacteria biomass have also been reported in low-nutrient alpine water bodies as opposed to nutrient-rich low-land systems (Taranu et al., 2015), suggesting the existence of other under-recognized factors contributing to the proliferation of harmful cyanobacteria.
Cyanobacteria are naturally targeted by a number of biological antagonists. In addition to the extensively studied effects of zooplankton grazing (Ger et al., 2016) or viral infections (Suttle, 1994), cyanobacteria are lethally parasitized by chytrids, a group of primitive aquatic fungi (phylum Chytridiomycota; Frenken et al., 2017). An increasing number of environmental molecular surveys have repeatedly reported a so-far disregarded diversity and widespread distribution of chytrids in aquatic ecosystems worldwide (e.g. Lefèvre et al., 2008, Hassett and Gradinger, 2016, Ortiz-Álvarez et al., 2018). Chytrid infection of phytoplankton is now considered an omnipresent phenomenon, which often reaches epidemic proportions (Frenken et al., 2017). As lethal parasites, chytrids control the abundance of their phytoplankton hosts and delay or even suppress bloom formation (Rasconi et al., 2012, Gerphagnon et al., 2015). In addition to direct effects on the timing and intensity of blooms, chytrid parasites seem to play more profound roles in the functioning of aquatic ecosystems, for instance by establishing alternative trophic pathways between primary and secondary production in aquatic food webs (Kagami et al., 2014, Agha et al., 2016) and promoting genetic diversity in phytoplankton populations (Gsell et al., 2013, Agha et al., 2018).
The use of fungicides has more than doubled since the 1950s. An estimated 300,000 tons of fungicides are used annually in agriculture worldwide to fight fungal pests and maximize food production (De et al., 2014). Maximum residual levels are usually set for these compounds to ensure consumer safety and plant protection. However, events such as overspray and drift lead to leaking of fungicides into nearby surface waters, potentially affecting non-target organisms, sometimes with unexpected outcomes (e.g. Rohr et al., 2017). Under controlled conditions, we tested the hypothesis that agricultural fungicides at environmentally relevant concentrations can indirectly promote harmful cyanobacterial blooms by inhibiting infection by their natural fungal antagonists.
Section snippets
Experimental setup
A laboratory experiment was conducted to analyze the effects of environmentally relevant concentrations of the agricultural fungicides tebuconazole (CAS nr. 107534-96-3), and azoxystrobin (CAS nr. 131860-33-8) on the spread of the chytrid parasite Rhizophydium megarrhizum (strain Chy-Kol2008; Sønstebø and Rohrlack, 2011) in populations of the toxic bloom-forming cyanobacterium Planktothrix rubescens (strain NIVA-CYA98), as well as on the growth of uninfected populations. Additionally, the
Results and discussion
The experiment confirmed the hypothesis that agricultural fungicides have the potential to promote the growth of cyanobacteria by inhibiting infection by their fungal parasites. Environmentally relevant concentrations of tebuconazole (20–200 μg/L) and azoxystrobin (1–30 μg/L) significantly reduced infection by chytrids (compared to controls without fungicides) without hampering cyanobacterial growth (Fig. 1a and b). These results strongly suggest that, under natural conditions, the sustained
Conflicts of interest
The authors declare no conflict of interest.
Contributions
RA conceived the experiment. All authors designed the experiment. BOC conducted the experiment and analyzed the data, with the help of RA. BOC wrote the initial version of the manuscript which was then reviewed and edited by JW and RA.
Acknowledgements
We are grateful to Dr. Thomas Rohrlack for supplying the chytrid strain. We thank Prof. Bruno B. Castro for advice on fungicide solution preparation and Mark Phillipo for proof reading. RA was supported by the Alexander von Humboldt Foundation and the Deutsche Forschungsgemeinschaft (DFG) grant AG284/1-1.
References (29)
- et al.
Neurotoxic cyanobacterial toxins
Toxicon
(2010) - et al.
The interaction between cyanobacteria and zooplankton in a more eutrophic world
Harmful Algae
(2016) - et al.
Accumulation of cyanobacterial toxins in freshwater “seafood” and its consequences for public health: a review
Environ. Pollut.
(2007) - et al.
Adaptation of a chytrid parasite to its cyanobacterial host is hampered by host intraspecific diversity
Front. Microbiol.
(2018) - et al.
Chytrid parasitism facilitates trophic transfer between bloom-forming cyanobacteria and zooplankton (Daphnia)
Sci. Rep.
(2016) - et al.
Worldwide pesticide use
Cyanobacteria-Toxins in Drinking Water
(2005)- et al.
Integrating chytrid fungal parasites into plankton ecology. Research gaps and needs
Environ. Microbiol.
(2017) - et al.
Using itraconazole to clear Batrachochytrium dendrobatidis infection, and subsequent depigmentation of Alytes muletensis tadpoles
Dis. Aquat. Org.
(2009) - et al.
Microbial players involved in the decline of filamentous and colonial cyanobacterial blooms with a focus on fungal parasitism
Environ. Microbiol.
(2015)
Comparison of sterol and fatty acid profiles of chytrids and their hosts reveals trophic upgrading of nutritionally inadequate phytoplankton by fungal parasites
Environ. Microbiol.
Chytrid epidemics may increase genetic diversity of a diatom spring-bloom
ISME J.
Chytrids dominate arctic marine fungal communities
Environ. Microbiol.
Cyanobacterial blooms
Nat. Rev. Microbiol.
Cited by (21)
Current trends and mismatches on fungicide use and assessment of the ecological effects in freshwater ecosystems
2024, Environmental PollutionStrobilurin fungicide increases the susceptibility of amphibian larvae to trematode infections
2024, Aquatic ToxicologyMoving beyond standard toxicological metrics: The effect of diclofenac on planktonic host-parasite interactions
2023, Aquatic ToxicologyCitation Excerpt :Understanding the sensitivity of chytrid parasite to diclofenac can only be feasible through changes in prevalence in our study. Ortiz-Cañavate et al. (2019) observed that fungicide, itraconazole at 100 and 1000 µg/L concentrations suppressed the spread of infection by chytrid parasite, Rhizophydium megarrhizum in cyanobacterium Planktothrix (Ortiz-Cañavate et al., 2019). A fungicide, thiophanate-methyl at 0.6 mg/L cleared Batrachochytrium dendrobatidis (chytrid fungus) infection in Lithobates sphenocephalus tadpoles (Hanlon et al., 2012).
Antiparasitic potential of agrochemical fungicides on a non-target aquatic model (Daphnia × Metschnikowia host-parasite system)
2022, Science of the Total EnvironmentCitation Excerpt :Available information about the impact of fungicides on aquatic fungal symbionts is considerably less comprehensive. So far, a few studies have demonstrated that common fungicides can reduce infectivity and parasite load in a yeast that parasitizes Daphnia (Cuco et al., 2017a, 2017b), as well as in chytrid species that infect tadpoles (Hanlon and Parris, 2012) and cyanobacteria (Ortiz-Cañavate et al., 2019). Analogously, decreased infestation and sporulation by commensal gut fungi were correlated with fungicide body burdens in black fly larvae (Wilson et al., 2014).