Intracellular bioaccumulation of the rare earth element Gadolinium in ciliate cells resulting in biogenic particle formation and excretion

Abstract Ciliates are abundant unicellular organisms capable of resisting high concentrations of metal ions in the environment caused by various anthropogenic activities. Understanding the cellular pathways involved in resistance to and detoxification of elements is required to predict the impact of...

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Main Authors: Jana Kohl, Michael Schweikert, Norbert Klaas, Marie-Louise Lemloh
Format: Article
Language:English
Published: Nature Portfolio 2023-04-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-023-32596-3
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author Jana Kohl
Michael Schweikert
Norbert Klaas
Marie-Louise Lemloh
author_facet Jana Kohl
Michael Schweikert
Norbert Klaas
Marie-Louise Lemloh
author_sort Jana Kohl
collection DOAJ
description Abstract Ciliates are abundant unicellular organisms capable of resisting high concentrations of metal ions in the environment caused by various anthropogenic activities. Understanding the cellular pathways involved in resistance to and detoxification of elements is required to predict the impact of ciliates on environmental element cycles. Here, we investigated the so far unknown process of tolerance, cellular uptake and bioaccumulation of the emerging rare earth element gadolinium (Gd) in the common ciliate Tetrahymena pyriformis. Gd treatment results in the intracellular formation and excretion of biogenic Gd-containing particles. This cellular process effectively removes dissolved Gd from the organic growth medium by 53.37% within 72 h. Based on light and electron microscopic observations, we postulate a detoxification pathway: Cells take up toxic Gd3+ ions from the medium by endocytosis, process them into stable Gd-containing particles within food vacuoles, and exocytose them. Stable biogenic particles can be isolated, which are relatively homogeneous and have a diameter of about 3 µm. They consist of the elements Gd, C, O, P, Na, Mg, K, and Ca. These findings broaden the view of metal ion accumulation by protists and are of relevance to understand environmental elemental cycles and may inspire approaches for metal recovery or bioremediation.
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spelling doaj.art-b44a336206bd472e8e839ab611bb3cf92023-04-09T11:12:25ZengNature PortfolioScientific Reports2045-23222023-04-0113111210.1038/s41598-023-32596-3Intracellular bioaccumulation of the rare earth element Gadolinium in ciliate cells resulting in biogenic particle formation and excretionJana Kohl0Michael Schweikert1Norbert Klaas2Marie-Louise Lemloh3Institute of Biomaterials and Biomolecular Systems, University of StuttgartInstitute of Biomaterials and Biomolecular Systems, University of StuttgartIWS, Research Facility for Subsurface Remediation (VEGAS), University of StuttgartSRF AMICA, University of StuttgartAbstract Ciliates are abundant unicellular organisms capable of resisting high concentrations of metal ions in the environment caused by various anthropogenic activities. Understanding the cellular pathways involved in resistance to and detoxification of elements is required to predict the impact of ciliates on environmental element cycles. Here, we investigated the so far unknown process of tolerance, cellular uptake and bioaccumulation of the emerging rare earth element gadolinium (Gd) in the common ciliate Tetrahymena pyriformis. Gd treatment results in the intracellular formation and excretion of biogenic Gd-containing particles. This cellular process effectively removes dissolved Gd from the organic growth medium by 53.37% within 72 h. Based on light and electron microscopic observations, we postulate a detoxification pathway: Cells take up toxic Gd3+ ions from the medium by endocytosis, process them into stable Gd-containing particles within food vacuoles, and exocytose them. Stable biogenic particles can be isolated, which are relatively homogeneous and have a diameter of about 3 µm. They consist of the elements Gd, C, O, P, Na, Mg, K, and Ca. These findings broaden the view of metal ion accumulation by protists and are of relevance to understand environmental elemental cycles and may inspire approaches for metal recovery or bioremediation.https://doi.org/10.1038/s41598-023-32596-3
spellingShingle Jana Kohl
Michael Schweikert
Norbert Klaas
Marie-Louise Lemloh
Intracellular bioaccumulation of the rare earth element Gadolinium in ciliate cells resulting in biogenic particle formation and excretion
Scientific Reports
title Intracellular bioaccumulation of the rare earth element Gadolinium in ciliate cells resulting in biogenic particle formation and excretion
title_full Intracellular bioaccumulation of the rare earth element Gadolinium in ciliate cells resulting in biogenic particle formation and excretion
title_fullStr Intracellular bioaccumulation of the rare earth element Gadolinium in ciliate cells resulting in biogenic particle formation and excretion
title_full_unstemmed Intracellular bioaccumulation of the rare earth element Gadolinium in ciliate cells resulting in biogenic particle formation and excretion
title_short Intracellular bioaccumulation of the rare earth element Gadolinium in ciliate cells resulting in biogenic particle formation and excretion
title_sort intracellular bioaccumulation of the rare earth element gadolinium in ciliate cells resulting in biogenic particle formation and excretion
url https://doi.org/10.1038/s41598-023-32596-3
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AT michaelschweikert intracellularbioaccumulationoftherareearthelementgadoliniuminciliatecellsresultinginbiogenicparticleformationandexcretion
AT norbertklaas intracellularbioaccumulationoftherareearthelementgadoliniuminciliatecellsresultinginbiogenicparticleformationandexcretion
AT marielouiselemloh intracellularbioaccumulationoftherareearthelementgadoliniuminciliatecellsresultinginbiogenicparticleformationandexcretion