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“Fungal Shunt”: Parasitic Fungi on Diatoms Affect Carbon Flow and Bacterial Communities in Aquatic Microbial Food Webs

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“Fungal Shunt”: Parasitic Fungi on Diatoms Affect Carbon Flow and Bacterial Communities in Aquatic Microbial Food Webs Characterizing the “fungal shunt”: Parasitic fungi on diatoms affect carbon flow and bacterial communities in aquatic microbial food webs Isabell Klawonna,1,2, Silke Van den Wyngaertb,3, Alma E. Paradaa, Nestor Arandia-Gorostidia, Martin J. Whitehousec, Hans-Peter Grossartb,d, and Anne E. Dekasa,2 aDepartment of Earth System Science, Stanford University, Stanford, CA 94305; bDepartment of Experimental Limnology, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, 12587 Berlin, Germany; cDepartment of Geosciences, Swedish Museum of Natural History, 104 05 Stockholm, Sweden; and dInstitute of Biochemistry and Biology, Potsdam University, 14476 Potsdam, Germany Edited by Edward F. DeLong, University of Hawaii at Manoa, Honolulu, HI, and approved March 26, 2021 (received for review February 3, 2021) Microbial interactions in aquatic environments profoundly affect Members of the fungal division Chytridiomycota, referred to global biogeochemical cycles, but the role of microparasites has as chytrids, can thrive as microparasites on phytoplankton cells in been largely overlooked. Using a model pathosystem, we studied freshwater (11, 13, 14) and marine systems (15–17), infecting up hitherto cryptic interactions between microparasitic fungi (chytrid to 90% of the phytoplankton host population (18–21). A recent Rhizophydiales), their diatom host Asterionella, and cell-associated concept, called mycoloop, describes parasitic chytrids as an in- and free-living bacteria. We analyzed the effect of fungal infections tegral part of aquatic food webs (22). Energy and organic matter on microbial abundances, bacterial taxonomy, cell-to-cell carbon are thereby transferred from large, often inedible phytoplankton transfer, and cell-specific nitrate-based growth using microscopy to chytrid zoospores, which are consumed by zooplankton (23–27). (e.g., fluorescence in situ hybridization), 16S rRNA gene amplicon Hence, parasitic chytrids establish a novel trophic link between sequencing, and secondary ion mass spectrometry. Bacterial abun- phytoplankton and zooplankton. Our understanding of element dances were 2 to 4 times higher on individual fungal-infected cycling and microbial interactions during chytrid epidemics, how- diatoms compared to healthy diatoms, particularly involving ever, remains sparse. For instance, the cell-to-cell C transfer from Burkholderiales. Furthermore, taxonomic compositions of both single phytoplankton cells to their directly associated chytrids has ENVIRONMENTAL SCIENCES diatom-associated and free-living bacteria were significantly differ- notbeenquantifiedtodate.Moreover,therelationshipbe- ent between noninfected and fungal-infected cocultures. The fungal tween parasitic chytrids and heterotrophic bacteria is largely microparasite, including diatom-associated sporangia and free- undescribed. swimming zoospores, derived ∼100% of their carbon content from the diatom. By comparison, transfer efficiencies of photosynthetic Significance carbon were lower to diatom-associated bacteria (67 to 98%), with a high cell-to-cell variability, and even lower to free-living bacteria Planktonic microorganisms interact with each other in multi- (32%). Likewise, nitrate-based growth for the diatom and fungi was farious ways, ultimately catalyzing the flow of carbon and synchronized and faster than for diatom-associated and free-living energy in diverse aquatic environments. However, crucial links bacteria. In a natural lacustrine system, where infection prevalence associated with eukaryotic microparasites are still overlooked reached 54%, we calculated that 20% of the total diatom-derived in planktonic networks. We addressed such links by studying photosynthetic carbon was shunted to the parasitic fungi, which can cryptic interactions between parasitic fungi, phytoplankton, be grazed by zooplankton, thereby accelerating carbon transfer to and bacteria using a model pathosystem. Our results demonstrate higher trophic levels and bypassing the microbial loop. The herein that parasitic fungi profoundly modified microbial interactions termed “fungal shunt” can thus significantly modify the fate of through several mechanisms (e.g., transferring photosynthetic photosynthetic carbon and the nature of phytoplankton–bacteria carbon to infecting fungi, stimulating bacterial colonization on interactions, with implications for diverse pelagic food webs and phytoplankton cells, and altering the community composition of global biogeochemical cycles. bacteria and their acquisition of photosynthetic carbon). Hence, fungal microparasites can substantially shape the microbially eukaryotic microparasites | phytoplankton–fungi–bacteria interactions | mediated carbon flow at the base of aquatic food webs and carbon fluxes should be considered as crucial members within plankton communities. arasitism is one of the most common consumer strategies on PEarth (1–3). Recently, it has also been identified as one of Author contributions: I.K., S.V.d.W., and A.E.D. designed research; I.K., S.V.d.W., A.E.P., the dominating interactions within the planktonic interactome N.A.-G., and M.J.W. performed research; H.-P.G. and A.E.D. contributed new reagents/ analytic tools; I.K. analyzed data; and I.K. and A.E.D. wrote the paper with the input from (4, 5), and yet parasites remain poorly considered in analyses of all coauthors. trophic interactions and element cycling in aquatic systems (6, 7). The authors declare no competing interest. The foundation of trophic interactions in plankton communities This article is a PNAS Direct Submission. is set by single-cell phytoplankton, which contributes almost half This open access article is distributed under Creative Commons Attribution License 4.0 of the world’s primary production (8). According to our common (CC BY). understanding, the newly fixed carbon (C) is channeled either 1Present address: Department of Biological Oceanography, Leibniz Institute for Baltic Sea through the microbial loop, classical food web, or viral shunt, Research, 18119 Rostock, Germany. which supports the growth of heterotrophic bacteria and nano- 2To whom correspondence may be addressed. Email: [email protected] or [email protected]. flagellates, zooplankton and higher trophic levels, or viruses, 3Present address: WaterCluster Lunz, Inter-University Center for Aquatic Ecosystem Re- respectively (9). However, fungi, particularly fungal microparasites, search, 3293 Lunz am See, Austria. are rarely considered as contributors to C and nutrient cycling, al- This article contains supporting information online at https://www.pnas.org/lookup/suppl/ though they are present and active in diverse aquatic environments doi:10.1073/pnas.2102225118/-/DCSupplemental. (10–12). Published May 31, 2021. PNAS 2021 Vol. 118 No. 23 e2102225118 https://doi.org/10.1073/pnas.2102225118 | 1of11 Downloaded by guest on September 27, 2021 Phytoplankton cells release substantial amounts of dissolved reactive phosphorous [SRP]). Concentrations of dissolved silica − organic C (DOC) (28), whereby up to 50% of photosynthetic C is (∼0.2 to 1.6 nmol · mL 1) were comparable on day 0 and 2 but consumed as DOC by bacteria (29–32). Thus, bacterial com- significantly higher in the infected treatment on day 6. Total − munities are intimately linked to phytoplankton abundances and DOC concentrations (∼70 to 140 nmol · mL 1) were equal in production (33). Phytoplankton–bacteria interactions are particu- both treatments on all sampling days, but on day 6, the 13C en- larly strong within the phycosphere, the region immediately sur- richment in the DOC pool was significantly higher in the infected rounding individual phytoplankton cells (33–35), where nutrient treatment (4.0 ± 0.4 versus 4.9 ± 0.0 13C atom percent [atom%] concentrations are several-folds higher compared to the ambient excess, P = 0.0001). DOC production rates were similar in both − − water (36, 37), and nutrient assimilation rates of phytoplankton- treatments (∼20 nmol C · d 1 · mL 1, SI Appendix, Table S2). associated bacteria are at least twice as fast as those of their free- living counterparts (38, 39). Importantly, parasitic chytrids may Bacterial Abundances, Community Composition, and Potential Activity. distort these phytoplankton–bacteria interactions within and out- Using fluorescence microscopy, we classified bacteria as 1) free- side the phycosphere since they modulate substrate and nutrient living bacteria and diatom-associated bacteria based on their at- availabilities and presumably also bacterial activity and community tachment to different types of Asterionella cells, including 2) composition. The effects of this distortion are virtually unresolved, noninfected, 3) infected, 4) postinfected, and 5) decaying cells but the few available data indicate that chytrid infections alter the (Fig. 1). Noninfected Asterionella were recognized as healthy, in- composition and concentration of DOC (40), while abundances of tact cells; infected Asterionella showed ongoing infections with a free-living bacteria increase (25, 40) or remain unchanged (24). mature epibiotic zoosporangium (herein sporangium); post- To disentangle phytoplankton–fungi–bacteria interactions at a infected Asterionella displayed remains of chytrid-related chitin microspatial single-cell scale—the scale at which phytoplankton, structures as a sign of previous infections after zoospore discharge; fungi, and bacteria intimately interact—we used one of the few and decaying cells showed low levels of autofluorescence but no existing model
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