Fate of Planktothrix-derived toxins in aquatic food webs: A case study in Lake Mindelsee (Germany)

Blooms of the red, filamentous cyanobacterium Planktothrix rubescens occur frequently in pre-alpine lakes in Europe, often with concomitant toxic microcystin (MC) production. Trophic transfer of MCs has been observed in bivalves, fish, and zooplankton species, while uptake of MCs into Diptera specie...

Full description

Bibliographic Details
Main Authors: Eva Riehle, Daniel G. Beach, Selina Multrus, Tarn Preet Parmar, Dominik Martin-Creuzburg, Daniel R. Dietrich
Format: Article
Language:English
Published: Elsevier 2024-03-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S014765132400229X
_version_ 1797261870521909248
author Eva Riehle
Daniel G. Beach
Selina Multrus
Tarn Preet Parmar
Dominik Martin-Creuzburg
Daniel R. Dietrich
author_facet Eva Riehle
Daniel G. Beach
Selina Multrus
Tarn Preet Parmar
Dominik Martin-Creuzburg
Daniel R. Dietrich
author_sort Eva Riehle
collection DOAJ
description Blooms of the red, filamentous cyanobacterium Planktothrix rubescens occur frequently in pre-alpine lakes in Europe, often with concomitant toxic microcystin (MC) production. Trophic transfer of MCs has been observed in bivalves, fish, and zooplankton species, while uptake of MCs into Diptera species could facilitate distribution of MCs into terrestrial food webs and habitats. In this study, we characterized a Planktothrix bloom in summer 2019 in Lake Mindelsee and tracked possible trophic transfer and/or bioaccumulation of MCs via analysis of phytoplankton, zooplankton (Daphnia) and emergent aquatic insects (Chaoborus, Chironomidae and Trichoptera). Using 16 S rRNA gene amplicon sequencing, we found that five sequence variants of Planktothrix spp. were responsible for bloom formation in September and October of 2019, and these MC-producing variants, provisionally identified as P. isothrix and/or P. serta, occurred exclusively in Lake Mindelsee (Germany), while other variants were also detected in nearby Lake Constance. The remaining cyanobacterial community was dominated by Cyanobiaceae species with high species overlap with Lake Constance, suggesting a well-established exchange of cyanobacteria species between the adjacent lakes. With targeted LC–HRMS/MS we identified two MC-congeners, MC-LR and [Asp3]MC-RR with maximum concentrations of 45 ng [Asp3]MC-RR/L in lake water in September. Both MC congeners displayed different predominance patterns, suggesting that two different MC-producing species occurred in a time-dependent manner, whereby [Asp3]MC-RR was clearly associated with the Planktothrix spp. bloom. We demonstrate an exclusive transfer of MC-LR, but not [Asp3]MC-RR, from phytoplankton into zooplankton reaching a 10-fold bioconcentration, yet complete absence of these MC congeners or their conjugates in aquatic insects. The latter demonstrated a limited trophic transfer of MCs from zooplankton to zooplanktivorous insect larvae (e.g., Chaoborus), or direct transfer into other aquatic insects (e.g. Chironomidae and Trichoptera), whether due to avoidance or limited uptake and/or rapid excretion of MCs by higher trophic emergent aquatic insects.
first_indexed 2024-03-07T19:43:52Z
format Article
id doaj.art-d8a2c69540604f2d983a1fe627087fb9
institution Directory Open Access Journal
issn 0147-6513
language English
last_indexed 2024-04-24T23:48:05Z
publishDate 2024-03-01
publisher Elsevier
record_format Article
series Ecotoxicology and Environmental Safety
spelling doaj.art-d8a2c69540604f2d983a1fe627087fb92024-03-15T04:42:53ZengElsevierEcotoxicology and Environmental Safety0147-65132024-03-01273116154Fate of Planktothrix-derived toxins in aquatic food webs: A case study in Lake Mindelsee (Germany)Eva Riehle0Daniel G. Beach1Selina Multrus2Tarn Preet Parmar3Dominik Martin-Creuzburg4Daniel R. Dietrich5University of Konstanz, Human and Environmental Toxicology Research Group, Universitaetsstrasse 10, Konstanz 78464, Germany; Corresponding authors.National Research Council Canada, Biotoxin Metrology, 1411 Oxford St., Halifax, Nova Scotia B3H 3Z1, CanadaUniversity of Konstanz, Human and Environmental Toxicology Research Group, Universitaetsstrasse 10, Konstanz 78464, GermanyBrandenburg Technical University (BTU), Cottbus-Senftenberg, Department of Aquatic Ecology, Seestrasse 45, Bad Saarow 15526, GermanyBrandenburg Technical University (BTU), Cottbus-Senftenberg, Department of Aquatic Ecology, Seestrasse 45, Bad Saarow 15526, GermanyUniversity of Konstanz, Human and Environmental Toxicology Research Group, Universitaetsstrasse 10, Konstanz 78464, Germany; Corresponding authors.Blooms of the red, filamentous cyanobacterium Planktothrix rubescens occur frequently in pre-alpine lakes in Europe, often with concomitant toxic microcystin (MC) production. Trophic transfer of MCs has been observed in bivalves, fish, and zooplankton species, while uptake of MCs into Diptera species could facilitate distribution of MCs into terrestrial food webs and habitats. In this study, we characterized a Planktothrix bloom in summer 2019 in Lake Mindelsee and tracked possible trophic transfer and/or bioaccumulation of MCs via analysis of phytoplankton, zooplankton (Daphnia) and emergent aquatic insects (Chaoborus, Chironomidae and Trichoptera). Using 16 S rRNA gene amplicon sequencing, we found that five sequence variants of Planktothrix spp. were responsible for bloom formation in September and October of 2019, and these MC-producing variants, provisionally identified as P. isothrix and/or P. serta, occurred exclusively in Lake Mindelsee (Germany), while other variants were also detected in nearby Lake Constance. The remaining cyanobacterial community was dominated by Cyanobiaceae species with high species overlap with Lake Constance, suggesting a well-established exchange of cyanobacteria species between the adjacent lakes. With targeted LC–HRMS/MS we identified two MC-congeners, MC-LR and [Asp3]MC-RR with maximum concentrations of 45 ng [Asp3]MC-RR/L in lake water in September. Both MC congeners displayed different predominance patterns, suggesting that two different MC-producing species occurred in a time-dependent manner, whereby [Asp3]MC-RR was clearly associated with the Planktothrix spp. bloom. We demonstrate an exclusive transfer of MC-LR, but not [Asp3]MC-RR, from phytoplankton into zooplankton reaching a 10-fold bioconcentration, yet complete absence of these MC congeners or their conjugates in aquatic insects. The latter demonstrated a limited trophic transfer of MCs from zooplankton to zooplanktivorous insect larvae (e.g., Chaoborus), or direct transfer into other aquatic insects (e.g. Chironomidae and Trichoptera), whether due to avoidance or limited uptake and/or rapid excretion of MCs by higher trophic emergent aquatic insects.http://www.sciencedirect.com/science/article/pii/S014765132400229XPlanktothrixCyanobacteria toxinsTrophic transferDeep chlorophyll maximumMicrocystin
spellingShingle Eva Riehle
Daniel G. Beach
Selina Multrus
Tarn Preet Parmar
Dominik Martin-Creuzburg
Daniel R. Dietrich
Fate of Planktothrix-derived toxins in aquatic food webs: A case study in Lake Mindelsee (Germany)
Ecotoxicology and Environmental Safety
Planktothrix
Cyanobacteria toxins
Trophic transfer
Deep chlorophyll maximum
Microcystin
title Fate of Planktothrix-derived toxins in aquatic food webs: A case study in Lake Mindelsee (Germany)
title_full Fate of Planktothrix-derived toxins in aquatic food webs: A case study in Lake Mindelsee (Germany)
title_fullStr Fate of Planktothrix-derived toxins in aquatic food webs: A case study in Lake Mindelsee (Germany)
title_full_unstemmed Fate of Planktothrix-derived toxins in aquatic food webs: A case study in Lake Mindelsee (Germany)
title_short Fate of Planktothrix-derived toxins in aquatic food webs: A case study in Lake Mindelsee (Germany)
title_sort fate of planktothrix derived toxins in aquatic food webs a case study in lake mindelsee germany
topic Planktothrix
Cyanobacteria toxins
Trophic transfer
Deep chlorophyll maximum
Microcystin
url http://www.sciencedirect.com/science/article/pii/S014765132400229X
work_keys_str_mv AT evariehle fateofplanktothrixderivedtoxinsinaquaticfoodwebsacasestudyinlakemindelseegermany
AT danielgbeach fateofplanktothrixderivedtoxinsinaquaticfoodwebsacasestudyinlakemindelseegermany
AT selinamultrus fateofplanktothrixderivedtoxinsinaquaticfoodwebsacasestudyinlakemindelseegermany
AT tarnpreetparmar fateofplanktothrixderivedtoxinsinaquaticfoodwebsacasestudyinlakemindelseegermany
AT dominikmartincreuzburg fateofplanktothrixderivedtoxinsinaquaticfoodwebsacasestudyinlakemindelseegermany
AT danielrdietrich fateofplanktothrixderivedtoxinsinaquaticfoodwebsacasestudyinlakemindelseegermany