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Effect of oxic and anoxic conditions on intracellular storage of polyhydroxyalkanoate and polyphosphate in Magnetospirillum magneticum strain AMB-1

Magnetotactic bacteria (MTB) are microorganisms widely inhabiting the oxic-anoxic interface of aquatic environments. Beside biomineralizing magnetic nanocrystals, MTBs are able to sequester various chemical elements (e.g., carbon and phosphorus) for the biogenesis of intracellular granules, like pol...

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Autores principales: Su, Qingxian, Andersen, Henrik Rasmus, Bazylinski, Dennis A., Jensen, Marlene Mark
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10310966/
https://www.ncbi.nlm.nih.gov/pubmed/37396362
http://dx.doi.org/10.3389/fmicb.2023.1203805
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author Su, Qingxian
Andersen, Henrik Rasmus
Bazylinski, Dennis A.
Jensen, Marlene Mark
author_facet Su, Qingxian
Andersen, Henrik Rasmus
Bazylinski, Dennis A.
Jensen, Marlene Mark
author_sort Su, Qingxian
collection PubMed
description Magnetotactic bacteria (MTB) are microorganisms widely inhabiting the oxic-anoxic interface of aquatic environments. Beside biomineralizing magnetic nanocrystals, MTBs are able to sequester various chemical elements (e.g., carbon and phosphorus) for the biogenesis of intracellular granules, like polyhydroxyalkanoate (PHA) and polyphosphate (polyP), making them potentially important in biogeochemical cycling. Yet, the environmental controls of intracellular storage of carbon and phosphorus in MTB remain poorly understood. Here, we investigated the influence of oxic, anoxic and transient oxic-anoxic conditions on intracellular storage of PHA and polyP in Magnetospirillum magneticum strain AMB-1. In the incubations with oxygen, transmission electron microscopy revealed intercellular granules highly rich in carbon and phosphorus, which were further interpreted as PHA and polyP based on chemical and Energy-Dispersive X-ray spectroscopy analysis. Oxygen had a strong effect on PHA and polyP storage in AMB-1 cells, as PHA and polyP granules accounted for up to 47 ± 23% and 5.1 ± 1.7% of the cytoplasmic space, respectively, during continuous oxic conditions, while granules disappeared in anoxic incubations. Poly 3-hydroxybutyrate (PHB) and poly 3-hydroxyvalerate (PHV) accounted for 0.59 ± 0.66% and 0.0033 ± 0.0088% of dry cell weight, respectively, in anoxic incubations, while the values increased by a factor of 7 and 37 after oxygen was introduced. The results highlight a tight link between oxygen, carbon and phosphorus metabolisms in MTB, where favorable oxic growth conditions can lead to metabolic induction of polyP and PHA granule biogenesis.
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spelling pubmed-103109662023-07-01 Effect of oxic and anoxic conditions on intracellular storage of polyhydroxyalkanoate and polyphosphate in Magnetospirillum magneticum strain AMB-1 Su, Qingxian Andersen, Henrik Rasmus Bazylinski, Dennis A. Jensen, Marlene Mark Front Microbiol Microbiology Magnetotactic bacteria (MTB) are microorganisms widely inhabiting the oxic-anoxic interface of aquatic environments. Beside biomineralizing magnetic nanocrystals, MTBs are able to sequester various chemical elements (e.g., carbon and phosphorus) for the biogenesis of intracellular granules, like polyhydroxyalkanoate (PHA) and polyphosphate (polyP), making them potentially important in biogeochemical cycling. Yet, the environmental controls of intracellular storage of carbon and phosphorus in MTB remain poorly understood. Here, we investigated the influence of oxic, anoxic and transient oxic-anoxic conditions on intracellular storage of PHA and polyP in Magnetospirillum magneticum strain AMB-1. In the incubations with oxygen, transmission electron microscopy revealed intercellular granules highly rich in carbon and phosphorus, which were further interpreted as PHA and polyP based on chemical and Energy-Dispersive X-ray spectroscopy analysis. Oxygen had a strong effect on PHA and polyP storage in AMB-1 cells, as PHA and polyP granules accounted for up to 47 ± 23% and 5.1 ± 1.7% of the cytoplasmic space, respectively, during continuous oxic conditions, while granules disappeared in anoxic incubations. Poly 3-hydroxybutyrate (PHB) and poly 3-hydroxyvalerate (PHV) accounted for 0.59 ± 0.66% and 0.0033 ± 0.0088% of dry cell weight, respectively, in anoxic incubations, while the values increased by a factor of 7 and 37 after oxygen was introduced. The results highlight a tight link between oxygen, carbon and phosphorus metabolisms in MTB, where favorable oxic growth conditions can lead to metabolic induction of polyP and PHA granule biogenesis. Frontiers Media S.A. 2023-06-15 /pmc/articles/PMC10310966/ /pubmed/37396362 http://dx.doi.org/10.3389/fmicb.2023.1203805 Text en Copyright © 2023 Su, Andersen, Bazylinski and Jensen. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Su, Qingxian
Andersen, Henrik Rasmus
Bazylinski, Dennis A.
Jensen, Marlene Mark
Effect of oxic and anoxic conditions on intracellular storage of polyhydroxyalkanoate and polyphosphate in Magnetospirillum magneticum strain AMB-1
title Effect of oxic and anoxic conditions on intracellular storage of polyhydroxyalkanoate and polyphosphate in Magnetospirillum magneticum strain AMB-1
title_full Effect of oxic and anoxic conditions on intracellular storage of polyhydroxyalkanoate and polyphosphate in Magnetospirillum magneticum strain AMB-1
title_fullStr Effect of oxic and anoxic conditions on intracellular storage of polyhydroxyalkanoate and polyphosphate in Magnetospirillum magneticum strain AMB-1
title_full_unstemmed Effect of oxic and anoxic conditions on intracellular storage of polyhydroxyalkanoate and polyphosphate in Magnetospirillum magneticum strain AMB-1
title_short Effect of oxic and anoxic conditions on intracellular storage of polyhydroxyalkanoate and polyphosphate in Magnetospirillum magneticum strain AMB-1
title_sort effect of oxic and anoxic conditions on intracellular storage of polyhydroxyalkanoate and polyphosphate in magnetospirillum magneticum strain amb-1
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10310966/
https://www.ncbi.nlm.nih.gov/pubmed/37396362
http://dx.doi.org/10.3389/fmicb.2023.1203805
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