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Temperature Response of Metabolic Activity of an Antarctic Nematode

SIMPLE SUMMARY: To understand how the McMurdo Dry Valleys of Antarctica (MCM) will respond to climate change, it is necessary to understand how dominant organisms in the ecosystem respond to fluctuations in temperature and water availability. We studied the effect of temperature on the metabolic act...

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Autores principales: Robinson, Colin Michael, Hansen, Lee D., Xue, Xia, Adams, Byron J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9855363/
https://www.ncbi.nlm.nih.gov/pubmed/36671801
http://dx.doi.org/10.3390/biology12010109
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author Robinson, Colin Michael
Hansen, Lee D.
Xue, Xia
Adams, Byron J.
author_facet Robinson, Colin Michael
Hansen, Lee D.
Xue, Xia
Adams, Byron J.
author_sort Robinson, Colin Michael
collection PubMed
description SIMPLE SUMMARY: To understand how the McMurdo Dry Valleys of Antarctica (MCM) will respond to climate change, it is necessary to understand how dominant organisms in the ecosystem respond to fluctuations in temperature and water availability. We studied the effect of temperature on the metabolic activity of Plectus murrayi, a widespread nematode in the MCM. By analyzing heat produced by metabolism along with CO(2) production and O(2) consumption, we found P. murrayi reaches peak metabolic activity at 40 °C, an unexpectedly high metabolic threshold for an Antarctic organism. As temperatures rise in the MCM, so too will the metabolic activity of P. murrayi. Such increases in energy demands have the potential to disrupt soil ecosystem structure and functioning, as the MCM system is carbon limited. Should P. murrayi experience heightened metabolic activity for extended periods of time, without additional carbon inputs the functioning of these soil ecosystems in the MCM may become significantly reduced. ABSTRACT: Because of climate change, the McMurdo Dry Valleys of Antarctica (MCM) have experienced an increase in the frequency and magnitude of summer pulse warming and surface ice and snow melting events. In response to these environmental changes, some nematode species in the MCM have experienced steady population declines over the last three decades, but Plectus murrayi, a mesophilic nematode species, has responded with a steady increase in range and abundance. To determine how P. murrayi responds to increasing temperatures, we measured metabolic heat and CO(2) production rates and calculated O(2) consumption rates as a function of temperature at 5 °C intervals from 5 to 50 °C. Heat, CO(2) production, and O(2) consumption rates increase approximately exponentially up to 40 °C, a temperature never experienced in their polar habitat. Metabolic rates decline rapidly above 40 °C and are irreversibly lost at 50 °C due to thermal stress and mortality. Caenorhabditis elegans, a much more widespread nematode that is found in more temperate environments reaches peak metabolic heat rate at just 27 °C, above which it experiences high mortality due to thermal stress. At temperatures from 10 to 40 °C, P. murrayi produces about 6 times more CO(2) than the O(2) it consumes, a respiratory quotient indicative of either acetogenesis or de novo lipogenesis. No potential acetogenic microbes were identified in the P. murrayi microbiome, suggesting that P. murrayi is producing increased CO(2) as a byproduct of de novo lipogenesis. This phenomenon, in conjunction with increased summer temperatures in their polar habitat, will likely lead to increased demand for carbon and subsequent increases in CO(2) production, population abundance, and range expansion. If such changes are not concomitant with increased carbon inputs, we predict the MCM soil ecosystems will experience dramatic declines in functional and taxonomic diversity.
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spelling pubmed-98553632023-01-21 Temperature Response of Metabolic Activity of an Antarctic Nematode Robinson, Colin Michael Hansen, Lee D. Xue, Xia Adams, Byron J. Biology (Basel) Article SIMPLE SUMMARY: To understand how the McMurdo Dry Valleys of Antarctica (MCM) will respond to climate change, it is necessary to understand how dominant organisms in the ecosystem respond to fluctuations in temperature and water availability. We studied the effect of temperature on the metabolic activity of Plectus murrayi, a widespread nematode in the MCM. By analyzing heat produced by metabolism along with CO(2) production and O(2) consumption, we found P. murrayi reaches peak metabolic activity at 40 °C, an unexpectedly high metabolic threshold for an Antarctic organism. As temperatures rise in the MCM, so too will the metabolic activity of P. murrayi. Such increases in energy demands have the potential to disrupt soil ecosystem structure and functioning, as the MCM system is carbon limited. Should P. murrayi experience heightened metabolic activity for extended periods of time, without additional carbon inputs the functioning of these soil ecosystems in the MCM may become significantly reduced. ABSTRACT: Because of climate change, the McMurdo Dry Valleys of Antarctica (MCM) have experienced an increase in the frequency and magnitude of summer pulse warming and surface ice and snow melting events. In response to these environmental changes, some nematode species in the MCM have experienced steady population declines over the last three decades, but Plectus murrayi, a mesophilic nematode species, has responded with a steady increase in range and abundance. To determine how P. murrayi responds to increasing temperatures, we measured metabolic heat and CO(2) production rates and calculated O(2) consumption rates as a function of temperature at 5 °C intervals from 5 to 50 °C. Heat, CO(2) production, and O(2) consumption rates increase approximately exponentially up to 40 °C, a temperature never experienced in their polar habitat. Metabolic rates decline rapidly above 40 °C and are irreversibly lost at 50 °C due to thermal stress and mortality. Caenorhabditis elegans, a much more widespread nematode that is found in more temperate environments reaches peak metabolic heat rate at just 27 °C, above which it experiences high mortality due to thermal stress. At temperatures from 10 to 40 °C, P. murrayi produces about 6 times more CO(2) than the O(2) it consumes, a respiratory quotient indicative of either acetogenesis or de novo lipogenesis. No potential acetogenic microbes were identified in the P. murrayi microbiome, suggesting that P. murrayi is producing increased CO(2) as a byproduct of de novo lipogenesis. This phenomenon, in conjunction with increased summer temperatures in their polar habitat, will likely lead to increased demand for carbon and subsequent increases in CO(2) production, population abundance, and range expansion. If such changes are not concomitant with increased carbon inputs, we predict the MCM soil ecosystems will experience dramatic declines in functional and taxonomic diversity. MDPI 2023-01-10 /pmc/articles/PMC9855363/ /pubmed/36671801 http://dx.doi.org/10.3390/biology12010109 Text en © 2023 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
Robinson, Colin Michael
Hansen, Lee D.
Xue, Xia
Adams, Byron J.
Temperature Response of Metabolic Activity of an Antarctic Nematode
title Temperature Response of Metabolic Activity of an Antarctic Nematode
title_full Temperature Response of Metabolic Activity of an Antarctic Nematode
title_fullStr Temperature Response of Metabolic Activity of an Antarctic Nematode
title_full_unstemmed Temperature Response of Metabolic Activity of an Antarctic Nematode
title_short Temperature Response of Metabolic Activity of an Antarctic Nematode
title_sort temperature response of metabolic activity of an antarctic nematode
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9855363/
https://www.ncbi.nlm.nih.gov/pubmed/36671801
http://dx.doi.org/10.3390/biology12010109
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