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First published online June 12, 2009
Journal of Experimental Biology 212, v-a (2009)
Copyright © 2009 The Company of Biologists Limited
doi: 10.1242/jeb.021519

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ELEVATED CO₂ PUTS WORMS ON THE SLOW TRACK TO A LONG LIFE

Jason E. Podrabsky

Portland State University

jpod{at}pdx.edu

Gas exchange is a basic requirement for almost all organisms, especially those that rely on aerobic metabolism, because mitochondria consume oxygen and produce carbon dioxide (CO₂) to produce ATP. Because of its critical importance to aerobic metabolism, the biology of oxygen has received a great deal of attention, and subsequently there is a tremendous body of information concerning the ways that cells sense and respond to changes in oxygen concentrations at organismal, organ, tissue and cellular levels. In contrast, far less attention has been paid to the biology of CO₂ in animals. However, CO₂ plays a critical role and is a major contributor to the regulation of pH in the extracellular fluids, and within cells. In fact, in mammalian systems ventilation patterns are largely regulated by levels of CO₂ in the blood and not oxygen. Despite the importance of CO₂ in mammalian physiology, very little work has focused on how cells sense levels of CO₂ and how they respond to elevated CO₂. Kfir Sharabi and colleagues recognized this deficiency in our knowledge and tested the effects of elevated CO₂ on the physiology, development and gene expression of the worm Caenorhabditis elegans.

To evaluate the affects of elevated CO₂ on organismal function, the team raised worms in normal air (0.04% CO₂) and air supplemented with 5, 9, 15 and 19% CO₂ at two temperatures, 20 and 25°C. The team then monitored larval development, egg production, egg survival, motility, life span and gene expression patterns using microarrays.

Elevated CO₂ slowed the rate of larval development, reduced the total number of embryos produced, and increased the worms' life span at concentrations of 9% or higher. The team also found the largest reduction in the number of embryos produced when the worms were continuously exposed to 19% CO₂ due to a decrease in the number of embryos produced by each individual after reaching adulthood. Exposing embryos to 19% CO₂ for discrete periods of time during development, the team found that the transition from the last larval stage (L4) to the adult stage is the most sensitive period of development in terms of the effects that elevated CO₂ had on each individual's subsequent reproductive output. Worms exposed to high CO₂ during this transition produced only 24% of the number of embryos produced by worms raised in normal air. Focusing on the long-term effects of CO₂ exposure, the team found that exposure to 15 and 19% CO₂ caused abnormal muscle development and reduced motility. Worms raised in 19% CO₂ also suffered a 40% drop in ATP levels compared with worms raised in normal air, indicating a significant physiological effect on metabolism that is presently unexplained.

Using gene expression profiling the team revealed hundreds of genes that change their expression during the first few hours of exposure to 19% CO₂. Elevated CO₂ appears to induce a stress response in C. elegans, where a small heat shock protein (hsp 12.3) is upregulated. Importantly, the patterns of gene expression associated with elevated CO₂ were different to those observed in worms exposed to hypoxia.

The results of this study indicate that elevated CO₂ has a profound affect on organismal form and function in this nematode worm. The unique nature of the response of C. elegans to elevated CO₂ suggests that in our quest to understand the importance of oxygen delivery, we may have been ignoring the critical other half of the gas exchange equation, the removal of CO₂.

References

Sharabi, K., Hurwitz, A., Simon, A. J., Beitel, G. J., Morimoto, R. I., Rechavi, G., Sznajder, J. I. and Gruenbaum, Y. (2009). Elevated CO₂ levels affect development, motility, and fertility and extend life span in Caenorhabditis elegans. PNAS 106,4024 -4029.[Abstract/Free Full Text]

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This Article Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Alert me to new issues of the journal Download to citation manager Google Scholar Articles by Podrabsky, J. E. PubMed Articles by Podrabsky, J. E. Social Bookmarking                         What's this?