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The Glacier Ice Worm, Mesenchytraeus solifugus, Elevates Mitochondrial Inorganic Polyphosphate (PolyP) Levels in Response to Stress
SIMPLE SUMMARY: Energy maintenance in living organisms is crucial for survival. The ice-obligate worm, Mesenchytraeus solifugus, displays an unusual bioenergetic pattern, namely that intracellular ATP levels increase with declining temperature. In this study, we address the effects of stress on mito...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
MDPI
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9774917/ https://www.ncbi.nlm.nih.gov/pubmed/36552279 http://dx.doi.org/10.3390/biology11121771 |
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author | Osorio, Teresa Scoma, Ernest R. Shain, Daniel H. Melissaratos, Diana S. Riggs, Lindsey M. Hambardikar, Vedangi Solesio, Maria E. |
author_facet | Osorio, Teresa Scoma, Ernest R. Shain, Daniel H. Melissaratos, Diana S. Riggs, Lindsey M. Hambardikar, Vedangi Solesio, Maria E. |
author_sort | Osorio, Teresa |
collection | PubMed |
description | SIMPLE SUMMARY: Energy maintenance in living organisms is crucial for survival. The ice-obligate worm, Mesenchytraeus solifugus, displays an unusual bioenergetic pattern, namely that intracellular ATP levels increase with declining temperature. In this study, we address the effects of stress on mitochondrial inorganic polyphosphate (polyP) and its relationship with ATP. Mitochondrial inorganic polyphosphate is a ubiquitous polymer whose role in the maintenance of prokaryotic and mammalian bioenergetics has been broadly demonstrated. We show here that polyP levels in ice worms increase with thermal stress, in contrast with those observed in other annelid worms. Thus, polyP may function as an energetic buffer in ice worms, effectively storing phosphate groups under stress and replenishing ATP under normal physiological conditions. ABSTRACT: The inorganic polymer, polyphosphate (polyP), is present in all organisms examined to date with putative functions ranging from the maintenance of bioenergetics to stress resilience and protein homeostasis. Bioenergetics in the glacier-obligate, segmented worm, Mesenchytraeus solifugus, is characterized by a paradoxical increase in intracellular ATP levels as temperatures decline. We show here that steady-state, mitochondrial polyP levels vary among species of Annelida, but were elevated only in M. solifugus in response to thermal stress. In contrast, polyP levels decreased with temperature in the mesophilic worm, Enchytraeus crypticus. These results identify fundamentally different bioenergetic strategies between closely related annelid worms, and suggest that I worm mitochondria maintain ATP and polyP in a dynamic equilibrium. |
format | Online Article Text |
id | pubmed-9774917 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | MDPI |
record_format | MEDLINE/PubMed |
spelling | pubmed-97749172022-12-23 The Glacier Ice Worm, Mesenchytraeus solifugus, Elevates Mitochondrial Inorganic Polyphosphate (PolyP) Levels in Response to Stress Osorio, Teresa Scoma, Ernest R. Shain, Daniel H. Melissaratos, Diana S. Riggs, Lindsey M. Hambardikar, Vedangi Solesio, Maria E. Biology (Basel) Article SIMPLE SUMMARY: Energy maintenance in living organisms is crucial for survival. The ice-obligate worm, Mesenchytraeus solifugus, displays an unusual bioenergetic pattern, namely that intracellular ATP levels increase with declining temperature. In this study, we address the effects of stress on mitochondrial inorganic polyphosphate (polyP) and its relationship with ATP. Mitochondrial inorganic polyphosphate is a ubiquitous polymer whose role in the maintenance of prokaryotic and mammalian bioenergetics has been broadly demonstrated. We show here that polyP levels in ice worms increase with thermal stress, in contrast with those observed in other annelid worms. Thus, polyP may function as an energetic buffer in ice worms, effectively storing phosphate groups under stress and replenishing ATP under normal physiological conditions. ABSTRACT: The inorganic polymer, polyphosphate (polyP), is present in all organisms examined to date with putative functions ranging from the maintenance of bioenergetics to stress resilience and protein homeostasis. Bioenergetics in the glacier-obligate, segmented worm, Mesenchytraeus solifugus, is characterized by a paradoxical increase in intracellular ATP levels as temperatures decline. We show here that steady-state, mitochondrial polyP levels vary among species of Annelida, but were elevated only in M. solifugus in response to thermal stress. In contrast, polyP levels decreased with temperature in the mesophilic worm, Enchytraeus crypticus. These results identify fundamentally different bioenergetic strategies between closely related annelid worms, and suggest that I worm mitochondria maintain ATP and polyP in a dynamic equilibrium. MDPI 2022-12-06 /pmc/articles/PMC9774917/ /pubmed/36552279 http://dx.doi.org/10.3390/biology11121771 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). |
spellingShingle | Article Osorio, Teresa Scoma, Ernest R. Shain, Daniel H. Melissaratos, Diana S. Riggs, Lindsey M. Hambardikar, Vedangi Solesio, Maria E. The Glacier Ice Worm, Mesenchytraeus solifugus, Elevates Mitochondrial Inorganic Polyphosphate (PolyP) Levels in Response to Stress |
title | The Glacier Ice Worm, Mesenchytraeus solifugus, Elevates Mitochondrial Inorganic Polyphosphate (PolyP) Levels in Response to Stress |
title_full | The Glacier Ice Worm, Mesenchytraeus solifugus, Elevates Mitochondrial Inorganic Polyphosphate (PolyP) Levels in Response to Stress |
title_fullStr | The Glacier Ice Worm, Mesenchytraeus solifugus, Elevates Mitochondrial Inorganic Polyphosphate (PolyP) Levels in Response to Stress |
title_full_unstemmed | The Glacier Ice Worm, Mesenchytraeus solifugus, Elevates Mitochondrial Inorganic Polyphosphate (PolyP) Levels in Response to Stress |
title_short | The Glacier Ice Worm, Mesenchytraeus solifugus, Elevates Mitochondrial Inorganic Polyphosphate (PolyP) Levels in Response to Stress |
title_sort | glacier ice worm, mesenchytraeus solifugus, elevates mitochondrial inorganic polyphosphate (polyp) levels in response to stress |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9774917/ https://www.ncbi.nlm.nih.gov/pubmed/36552279 http://dx.doi.org/10.3390/biology11121771 |
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