The Artful Amoeba

The Artful Amoeba

A Blog About the Weird Wonderfulness of Life on Earth

Shimmying Sheet Animals Sense Oxygen With Enzymes That Still Work in You


Smooth Operator: the slinky placozoan Trichoplax adhaerans. Creative Commons Oliver Voigt. Click image for license and link.

Author's Note: This post is being entered in the National Evolutionary Synthesis Center ScienceOnline 2012 Travel Award contest. Enjoy!

Hidden away in calm, sheltered coastal waters is a remarkable little animal: a tiny transparent sheet of cells called a placozoan. Though composed of only a few thousand cells and no more than 25 micrometers thick (a bacterium is about 1 micromter thick), it's an animal -- the simplest we know of.

Here's one in action:

And hidden inside it, scientists found recently, may be a clue to the Cambrian Explosion.

The Cambrian Explosion, you will recall, was the sudden appearance of the major modern groups of complex animals around 550 million years ago after several billion years of unmolested microbial partying on Planet Earth. Then, suddenly, Big Life crashed the party. What happened?

Placozoans, which may resemble the first animals, wander about eating algae and other detritus. Both upper and lower surfaces bear flagella that the creature uses to swim around. The whole organism can glue itself to a feeding surface and arch upward to form a makeshift stomach into which it excretes digestive enzymes. It then swallows the resulting goo through cellular drinking called pinocytosis.

Here's a diagram (in French)*:

Public Domain. Click image for link.

And here is Trichoplax feeding behavior in action. Whatever genius thought to put this music with this video, well, I salute you.

The Atavism had a great post on placozoans a few months ago that is well worth reading if you'd like to learn more about their basic biology.

Though these little creatures look about as dissimilar to humans as can be, we do, in fact, share quite a few similarities. Nearly 87% of its 11,500+ protein-coding genes are identifiably similar to genes in other animals. And interestingly enough, scientists have just discovered that Trichoplax contains something else in common with us and all other animals, but not any other life: special oxygen sensors.

While the Cambrian explosion was under way, oxygen concentrations were rising. For most of Earth's history, atmospheric oxygen concentrations had not exceeded perhaps 3%. Early single-celled organisms just absorbed oxygen by diffusion. That made it hard for organisms that dared form layers of cells greater than one or two thick to breathe, because there was no way enough oxygen could diffuse to interior cells.

But in a world where atmospheric oxygen concentrations were busy rising from 3% to near-modern levels of about 21%, oxygen could diffuse much further. That in of itself may have helped drive the appearance of multicellular life. But that solution only goes so far.

A related problem for any such multicellular organism is how to know whether the cells inside are starving for oxygen or in danger of overload. Unattended oxygen is a bit like a bad drunk: it staggers around and breaks things. Too much of it in the cell can lead to a buildup of toxic reactive oxygen chemicals. On the other hand, hypoxia, or oxygen starvation, is a bad situation too. Without an oxygen-sensing system, cells have no way of taking action to prevent suffocation or poisoning.

Trichoplax adhaerens, stained and under the confocal microscope, by Karolin von der Chevallerie (Schierwater lab, University of Hannover). Used with permission.

But this is just what scientists in the UK and Germany have discovered in placozoans. In animals studied so far, scientists have found three critical oxygen-sensing proteins: an oxygen sensing protein called proline hydroxylase domain enzyme (PHD), a hypoxia response protein called hypoxia-inducible transcription factor (HIF) that can be switched on or off by PHD, and a trash-tagging protein called von Hippel Lindau protein (VHP -- love that name).

When PHD senses oxygen, it switches off HIF by adding -OH (hydroxyl) units to certain proline amino acids near the end of the protein and VHP then tags it for trashing(by ubiquitination). When PHD does not sense oxygen, it doesn't tag HIF, and HIF -- a transcription factor -- is transported back to the nucleus where it promotes the production of a gene that shuts off the Citric Acid Cycle (a system that cells use to harness oxygen to extract lots of energy from glucose) along with a host of other oxygen-related genes. As a result, glucose is shunted from the Citric Acid cycle into the energetically-less-productive but undoubtedly-preferable-to-starving process of fermentation.

What Loenarz et al. found and published in EMBO Reports last January was that the basic components of this system -- present in more elaborate forms in humans and all other animals tested -- is present even in placozoans, and still functioning much as it does in humans.

Stained, fluorescent T. adhaerans under the confocal microscope. Staining is for the Hox-Para-Hox gene Trox-2. Image by Karolin von der Chevallerie (Schierwater lab, University of Hannover).

In fact, when they inserted the placozoan version of the oxygen sensor PHD into human cells, it worked just as well as human forms in shutting off the hypoxia-response protein HIF. Think about that: the functioning of these proteins is so conserved (read: important) that they still work in species separated by at least 550 million years of evolution. Wow.

So what could this mean? The HIF system is not found in single-celled protists or the choanoflagellate Monosiga brevicollis, which, as I mentioned in my last post on sponges, are probably animals' closest relatives. That means that early on, animals came up with a way to maintain oxygen homeostasis within their enlarging bodies. Such a system gave them a way to sense whether cells inside them needed oxygen, and then take appropriate measures.

It was a system so successful we are all still using it, and with genes so similar to our animal relatives -- even to shimmying microbial sheet animals -- we could all basically still trade with each other. You could probably swap in the T. rex oxygen sensing system, were you to know it, and get along just fine (and impress every five-year-old on the planet).Thus, the first animals, whatever they looked like, probably cobbled together this system during the oxygen-fueled Cambrian bloom, and in the process, helped propel themselves to half a billion years of evolutionary success.

Loenarz C, Coleman ML, Boleininger A, Schierwater B, Holland PW, Ratcliffe PJ, & Schofield CJ (2011). The hypoxia-inducible transcription factor pathway regulates oxygen sensing in the simplest animal, Trichoplax adhaerens. EMBO reports, 12 (1), 63-70 PMID: 21109780

Rytkönen KT, & Storz JF (2011). Evolutionary origins of oxygen sensing in animals. EMBO reports, 12 (1), 3-4 PMID: 21109778


*I hereby move that a suitable French restaurant in New York City be renamed "Chez Trichoplax". In order to dine, however, you have to hover over your food and digest it by absorption. I'd eat there.



The views expressed are those of the author and are not necessarily those of Scientific American.

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