Climate Change Developmental Biology Ocean Acidification Physiology

Sea urchins work harder, faster to cope with ocean acidification

Francis Pan T.-C., Applebaum S.L., and Manahan D.T. Experimental ocean acidification alters the allocation metabolic energy. PNAS. 14 April 2015. doi: 10.1073/pnas.1416967112

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You’re lying on chaise lounge on a cruise ship somewhere in the tropics sipping a cocktail and working on your tan. Suave bossa nova drifts sensuously through the sultry air, and you let out sigh of satisfaction — sweet escape. Suddenly over the loud speaker the captain announces, “ladies and gentleman – the ship is sinking.” “Besa mi mucho” is drowned out by panicked commotion. A glass shatters on the deck. Babies cry. The heat is suddenly unbearable. “But, please, relax and enjoy the rest of your stay,” continues the captain. “The crew is working overtime to keep us afloat.” Indeed, every last crew member is down below frantically filling and emptying buckets of water overboard. With such reassurances, the cruise continues in relative peace, but the chef and the maids have also had to pitch into the bailing effort, so you’re left with vending machine dinners and dirty sheets for the rest of your holiday.

In much the same way as your cruise ship was able to maintain its restful course, sea urchins challenged with ocean acidification are able to redirect their energy resources to achieve normal development according to a recent study by Francis Pan et al. published in the Proceedings of the National Academy of Sciences. However, re-budgeting energy resources comes at a cost to the fitness of the organism, highlighting a potential consequence to marine life posed by man-made ocean acidification due to industrial emissions of carbon dioxide, also the main culprit of global warming.

Francis Pan et al. examined the effects of acidification on high-level parameters such as metabolism (energy consumption), larval size, and gene expression, in addition to monitoring physiological processes such as protein synthesis and ion transport, which consume most of the cell’s energy during development. They measured these parameters for laboratory reared larvae over a ten day period of development, comparing larvae raised under current ocean conditions to those raised under the lower limit near-future projections for ocean acidification put forth by the International Panel on Climate Change.

They initially examined effects of acidification on morphology of developing larvae, and found no change in body length between treated and untreated larvae. Additionally, they assessed size-specific metabolic activity, as determined by oxygen consumption, and found no effect for treated versus untreated larvae. Hence, it would appear that sea urchins are able to maintain normal development under acidification.

All good, by the looks of things. No change in metabolism (A)  or body length (B) were observed between treated (hollow symbols) and untreated (black symbols) larva.
All good, by the looks of things. No changes in body length for different aged larva (A) or body length versus metabolism (B) were observed between treated (hollow symbols) and untreated (black symbols) larva. (Francis Pan et al., 2015)

Yet, as Francis Pan et al. soon found out, not all was well in the sea urchin cell. Proteins are the workhorses of every cell without which the chemical reactions that make life would come to a screeching halt. Moreover, protein synthesis is an energetically expensive process and hence important for assessing the changes in energy usage in developing larvae resulting from acidification. They observed elevated rates of protein synthesis in the sea urchin larvae under acidification despite no change in overall protein content. Furthermore, they noted an identical protein fingerprint for treated versus untreated larvae, suggesting that the overall process of protein synthesis was made less efficient by acidification. In other words, under acidification, more energy was being expended to yield the same levels and kinds of protein.

protein content and synthesis rate
Working harder to achieve the same. While no change was observed for protein content versus body size (A) for treated (hollow symbols) as compared untreated (black symbols), rates of protein synthesis increased drastically between the experimental and the control (B). (Francis Pan et al., 2015)

In addition to elevated rates of protein synthesis, Francis Pan et al. observed a two-fold increase in the activity of ion transporters that utilize chemical energy in the form of adenosine triphosphate (ATP) to pump sodium and potassium across the cell membrane. Ion transporters are important for signaling in development, and may play a role in regulating the acidity inside the cell. Notably, the increase in activity was only observed through direct measurements of ion transport, and could not be predicted through measurement of gene expression or gross biochemical activity. Hence, Francis Pan et al. emphasize the importance of physiological measurements in understanding the effects ocean acidification, which would otherwise be lost by indirect measures such as gene expression, and holistic measurements such as overall metabolism.

Pumping ions.
Pumping ions.  A) Increased rates of ion transport under acidification (solid line) versus control conditions (dashed line). B) Body length versus ion transport activity shows an average of 1.4-fold increase in size-specific ion transport rates. C) Gene expression does not predict the increase in ion transport activity. (Francis Pan et al., 2015)

Interpreting their observations, Francis Pan et al. translated marginal increases in the rate of protein synthesis and ion transport activity into changes in the energy (ATP) budget of the cell. They estimated a nearly 30 percent increase in the cell’s allocation of ATP toward protein synthesis and ion transport under acidifying conditions in growing larvae. Changes in allocation of ATP mean loss of capacity to respond to other environmental stressors. For example, transporters required for removal of environmental toxins known as ABC transporters (for ATP binding cassette) rely directly on energy from ATP to physically pump toxins out of the cell.

Breaking the ATP bank. Changes in allocation of ATP to protein synthesis (black) and ion transport activity (grey) for control versus acidified larva over a 10-day period of development.
Breaking the ATP bank. Changes in allocation of ATP to protein synthesis (black) and ion transport activity (grey) for control versus acidified larvae over a 10-day period of development.

In describing physiological effects of global warming on sea urchin development, Francis Pan et al. stress the importance of a holistic view for studying effects of stressors at sub-lethal levels. While gene expression, biochemistry, and gross morphological characteristics all said the organism was doing just fine, cellular level physiology told of an organism working overtime to make ends meet. Sea urchins are important ecological players, whose grazing behavior prevents algae and grasses from overrunning their intertidal habitats. Hence, ocean acidification might not only signal disaster for a single species, but could also lead to cascade effects resulting in the destruction of entire ecosystems.

While organisms might be giving us some leeway in re-allocating their energy resources to stay alive, we must curb our carbon dioxide emissions to avoid the tipping point of ocean acidification that triggers a mass extinction of marine life. The crew can only keep the cruise ship afloat for so long with buckets.


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