American Society of Naturalists

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"Partitioning the Apparent Temperature Sensitivity into Within- and Across-Taxa Responses: Revisiting the Difference between Autotrophic and Heterotrophic Protists"

Posted on by Danilo Giacometti

Bingzhang Chen (陈炳章), David J. S. Montagnes, Qing Wang (王庆), Hongbin Liu (刘红斌), and Susanne Menden-Deuer, April 2023

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Hotter is partially better? New work reveals that autotrophs and heterotrophs may be similarly sensitive to temperature increases

Groovy ciliates. Photo credit: David Montagnes
Groovy ciliates. Photo credit: David Montagnes

Understanding how warming temperatures affect different kinds of organisms helps scientists predict how impending climate change will impact biodiversity. Temperature influences virtually all physiological functions, including metabolism and respiration. However, temperature may impact these functions differently in groups of organisms that metabolize nutrients and respire differently. Autotrophs such as plants and algae produce their own food through light, water, and chemicals (usually carbon dioxide). In contrast, heterotrophs such as animals and fungi obtain energy by eating other organisms. Additionally, autotrophs and heterotrophs respire —a common measure of energy expenditure—differently. Briefly, autotrophs intake CO2 and release O2, whereas heterotrophs intake O2 and release CO2. Increased temperatures lead to increased respiratory rates and consequently increased metabolic rates in both autotrophs and heterotrophs. Hence, climate change is likely to affect how these organisms maintain energetic equilibrium. For years, conventional analysis showed that heterotrophs were more sensitive to changes in temperature than autotrophs. This suggests that the metabolism of heterotrophs should increase more rapidly than that of autotrophs as temperatures rise, which may lead to dramatic food web and ecosystem changes.

While the scientific literature has largely accepted the notion that autotrophs are less thermally sensitive than heterotrophs, certain confounding factors need to be considered and addressed, such as controlling for variation within taxonomic groups. This is precisely the impetus behind the work of Chen et al. (2023), who developed a mathematical framework that partitions within- and across-taxa thermal sensitivities in protists, a kingdom of life encompassing both autotrophic and heterotrophic members. Through this approach, the authors identified that 92% of differences in the thermal sensitivity of autotrophs and heterotrophs could be explained by within-taxa responses.

In addition, Chen et al. (2023) showed that the extent to which thermal sensitivities differ among species was similar between autotrophs and heterotrophs. This is relevant, as it lends support to the “hotter-is partially-better” hypothesis as a potential mechanism behind the pattern retrieved by the authors. This hypothesis posits that maximal growth rates should increase with temperature, but adaptation of biochemical reactions is still partially limited by thermodynamics. Thus, while hotter is better in general, there are limits to thermal adaptation that impact all species regardless of their metabolism. In this sense, autotrophs and heterotrophs have a similar capacity to adapt to changing thermal regimes.

Through their work, Chen et al. (2023) showed that the current appreciation of lower temperature sensitivity in autotrophs compared to heterotrophs arose due to reductionist approaches that failed to control for within- and among-species trends. Importantly, the partitioning methodology employed in this study is readily applicable to any linear regression analysis that involves grouping. Thus, while the current study provides a step towards a more complete understanding of thermal adaptation in the context of energetics, the framework of Chen et al. (2023) can be applied in contexts ranging from phylogenetic analyses to comparisons between ecosystems.


Abstract

Conventional analyses suggest that the metabolism of heterotrophs is thermally more sensitive than that of autotrophs, implying that warming leads to pronounced trophodynamic imbalances. However, these analyses inappropriately combine within- and across-taxa trends. Our new analysis separates these, revealing that 92% of the difference in the apparent thermal sensitivity between autotrophic and heterotrophic protists does indeed arise from within-taxa responses. Fitness differences among taxa adapted to different temperature regimes only partially compensate for the positive biochemical relationship between temperature and growth rate within taxa, supporting the hotter-is-partially-better hypothesis. Our work highlights the importance of separating within- and across-taxa responses when comparing temperature sensitivities between groups, which is relevant to how trophic imbalances and carbon fluxes respond to warming.

分离种内和种间的温度敏感性:重新审视自养和异养单细胞真核生物的差异

 

传统研究认为异养生物代谢速率相比自养生物而言对温度变化更加敏感,因此升温会增强自养和异养过程的不平衡。然而,之前研究未曾合理区分种内和种间对温度响应的差异。本研究提出一种新的方法分离种内和种间对温度的不同响应,发现自养和异养单细胞真核生物的表观温度敏感性(活化能)的差异主要(92%)来自于种内关系。不同种对温度的适应提高了它们的生长率;然而此生长率的提高只能部分抵消种内温度对生长率的影响。本研究揭示了在比较不同生物之间温度敏感性时区分种内和种间关系的重要性。


Danilo Giacometti in the field.<br/>Photo credit: Danilo Giacometti
Danilo Giacometti in the field.
Photo credit: Danilo Giacometti

Author Bio:

 

Danilo Giacometti is a PhD student at Brock University, ON, Canada. He is an eco-physiologist who focuses on understanding how organisms respond to environmental change on temporal scales. He studies aspects that are vital to organismal functioning, such as thermoregulation and energetics. Vertebrate ectotherms are his main study system, with a special emphasis on amphibians and non-avian reptiles.