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These Fish Have Nose Turbines

Zebra_fish.jpg

We see turbines in wind farms, in generators, and in jet engines. Run a Google search on “turbine” and look at the images. You can’t find any that look like random accidents. Instead, almost as a rule, they appear downright elegant, highly sophisticated, and complex. Well, here’s a “turbine” inside the nose of a tiny fish. It is no exception.

In Current Biology, a dozen researchers from Europe and Japan tell an amazing story about what they found in four-day-old zebrafish larvae. They actually use the word turbine:

Our data showed for the first time how the motile cilia decorating the nose pit act as a very powerful water turbine and generate strong and robust flow fields that allow fish to quickly exchange the content of the nose. Importantly, this mechanism increases the sensitivity and temporal resolution of odor computations both in stagnant and running aquatic environments and does not require muscle contraction. [Emphasis added.]

Earlier in the paper, they refer to “these microscopic jet turbines” that help fish smell better. (Especially after a few days in the fridge. Ha ha. Thanks, folks, we’ll be here all week.)

The paragraph quoted above refers to “motile cilia” which, incidentally, “Revolutionary” biochemist Michael Behe used as illustrations of irreducibly complex molecular machines in Darwin’s Black Box twenty years ago (pp. 59ff) and in more detail in The Edge of Evolution (2007, Chapter 5). There are also non-motile cilia — just as complex — that work as sensory antennae on most vertebrate cells. The motile cilia, by contrast, are fun to watch, because they move like whips. The hair-like projections on ciliated cells slide along the membrane for the wind-up, then extend fully for a power stroke. This goes on in your windpipe right now, sweeping dust out and keeping your airways clean. The cilia beat in a coordinated fashion, creating waves that collectively move particles along a train of flow, more powerful than a single cilium could accomplish alone. No one knows how they do that (e.g., Live Science).

If you recall the animation of salmon olfaction in Illustra’s film Living Waters (watch it again here), you remember seeing non-motile cilia rising out of the olfactory epithelium, the tissue inside the nose. Those are the cilia on olfactory receptor neurons (ORNs) that latch onto odorant molecules and send the information down molecular “wires” (neurons) to the olfactory bulb (OB). In the olfactory bulb, the collected information is sorted into combinatorial codes that classify tens of thousands of different odorants before sending the processed information to the brain.

What the film doesn’t show is what this paper now reveals. Surrounding the epithelium are cells with motile cilia. Beating in synchrony, they create a flow of water, just like a turbine. This dynamic flow — requiring no muscles — accomplishes several functions. First, it draws water into the nose, even in stagnant water or when the fish is idle. Second, it creates a flow pattern that directs odorant molecules over the sensory neurons and then out to the sides. This increases the sensitivity of the sense of smell dramatically. Third, the flow pattern helps the fish detect changes in odor patterns much more rapidly than it could otherwise (i.e., it increases the temporal resolution of the fish’s sense of smell). The paper’s title sums this up: “Motile-Cilia-Mediated Flow Improves Sensitivity and Temporal Resolution of Olfactory Computations.”

Computations? Yes, that’s what goes on in the fish’s brain as it processes the combinatorial codes sent from the olfactory bulb. Visualize that salmon swimming upriver, trying to follow a faint trail of odor molecules on its way to its natal stream. Obviously, the eager fish can do a better job of computation if the information comes in faster. The ciliary turbine helps the fish turn up its response time, whether it’s hanging out idle or swimming rapidly to get home.

Our measurements showed that fluctuating odor stimuli with decreasing inter-stimulus intervals are sampled significantly faster and with higher temporal resolution at the nose pits of controls [wild-type fish]…. In line with these findings, we observed that odor fluctuations are encoded significantly better at the level of the olfactory bulbs at all inter-stimulus intervals by control animals…. In fact, increasing the difficulty of the task by challenging the animals with faster odor fluctuations led to more significant differences in temporal encoding of odors by the OB neurons of control animals….

Young zebrafish provide an ideal way to observe this, because when the larvae are about four days old, their noses are shaped like little cups. It’s one of the few places in nature where scientists can watch motile cilia at work in a live animal. In a series of clever experiments, the researchers set out to test the hypothesis that fish smell better with cilia turbines. They used wild-type as controls, and mutants without motile cilia for testing.

  • Do the motile cilia beat with a measurable frequency? Check. Yes, about 25 Hz.

  • Do the cilia cooperatively draw water into the nose? Check.

  • Does the flow pattern draw particles over the olfactory neurons? Check.

  • What is the average dwell time of an odorant on the epithelium? About 0.4 seconds.

  • Where does the flow go after flowing over the epithelium? Out to the sides.

  • Is the flow pattern caused by the motile cilia? Check. Mutants with paralyzed cilia lack the flow pattern.

  • Is a similar turbine system found in young salmon? Check; it’s not unique to zebrafish.

  • Does the flow pattern increase activity in the olfactory bulb? Check. Passive diffusion of odors had a much lower response in the mutant fish.

  • Is the response better when an artificial flow is introduced into the nose? No; mutant fish can respond just as well to water flowing into the nose, but they suffer in stagnant water or when not swimming. Moreover, the dwell time of each odorant is increased, reducing temporal resolution.

  • Do rapidly fluctuating odor plumes introduced into the water show up in the OB? Check. The flow pattern appears to increase the temporal sensitivity to rapidly changing odor plumes. When pulses of odors are introduced every 2, 4, or 8 seconds, the response changes accordingly in wild-type. Mutants, however, suffer a delay in odor arrival and have longer odorant dwell times, decreasing temporal resolution in dynamic environments.

Here’s how they summarize their main findings:

Thanks to the optical accessibility of zebrafish nose pit, we could fully characterize how motile cilia beat to generate a robust flow in an intact organism. First, the asymmetric beating pattern that we show for the motile cilia of the nose is conserved across many MCCs [multi-ciliated cells] located along the brain ventricles, spinal cord, and respiratory tract. Second, the average CBF [cilia beat frequency] of zebrafish and salmon olfactory MCCs is rather uniform across individuals and lies between 19 and 30 Hz…. Third, we showed that flow characteristics resulting from the specific location and asymmetric beating of motile cilia are tailored to the organ’s need. In the brain ventricles, beating cilia can concentrate molecules locally or prevent entry to another ventricular area by generating boundaries. Our findings suggest here that the robust and directional flow, generated by motile cilia in the nose pit, guarantees an efficient exposure of ORNs to odors but for a restricted time. Even though it is now clear that fluid dynamics are regulated by the power and directionality of ciliary beating, the cellular and molecular mechanisms underlying the establishment of asymmetric ciliary beating remain to be fully understood.

So after twenty years, Behe will still have more to write about these amazing molecular machines. The researchers point out that similar principles may operate in mammals and humans. You, too, could have turbines in your nose… wind turbines!

The authors introduce evolutionary speculations at several points. For one, they make a big deal of the fact that motile cilia show up all over the place: in the brain, in the airways, and in fish noses.

It is an intriguing correlation that the motile cilia in the nose of most vertebrates and in the airways of mammals generate ciliary beating with similar principles, highlighting a possible evolutionary relationship between these structures.

Yet they have to admit that cilia are “conserved across most vertebrate species from fish to rodents.” That’s not evolution; that’s stasis. For another piece of evidence, they point out differences between zebrafish and more “primitive” creatures:

As an alternative solution, a few aquatic vertebrates evolved accessory sacs in their olfactory organs that can be expended and compressed. Lobsters were shown to move their antennules to draw water into the olfactory epithelium.

Later in the paper:

Interestingly, in hagfish and lampreys, which are considered evolutionarily primitive fish species, the respiratory flow initiated by the velum contraction passes through the olfactory chamber toward the gills and thus draw odors. Thus, from an evolutionary perspective, it appears that cilia-driven flow in the nose pit is rather novel and may underlie a powerful and energy-efficient mechanism to draw odors into the nose. Altogether, we propose that this mechanism might have evolved to facilitate better sampling of dynamically changing odor plumes and thereby enhance the temporal resolution of olfactory computations.

There are at least two difficulties here. One is that different mechanisms that achieve a common function make the problem worse for Darwinian evolution. It multiplies the number of chance mutations that had to be selected. Another is the statement that a “mechanism might have evolved to” do something useful. Darwinian evolution has no foresight. It has no goal. It cannot order and direct mutations to conspire to work together to create a novel “powerful and energy-efficient mechanism,” particularly one as irreducibly complex as a cilium. The authors don’t even begin to address the complexity of a single cilium.

The irreducible complexity doesn’t stop there. The cilia in a tissue have to work in concert. They have to line up in certain locations in the nose to create the flow pattern. And the brain has to be tuned to respond rapidly enough to the increased rate and lower dwell times of each odorant. The authors are fully aware, furthermore, that damaged cilia cause serious problems, just as they did with the cilia-defective mutant fish.

Cilia are microscopic hair-like structures extending from the surface of almost all cells of the vertebrate body. Motile cilia actively move and drive directional flow patterns across tissues, whereas primary cilia are enriched in receptors and play crucial sensory roles. It is therefore not surprising that mutations affecting the structure, function, or presence of cilia result in multiple human pathologies, collectively known as ciliopathies.

These evolutionary speculations aside (which, by the way, stand in contrast to their exemplary lab work), we can step back and appreciate this new discovery that adds another level of complexity and elegance to what we already knew about fish olfaction. Are turbines intelligently designed? Try to think of one that isn’t.

Photo: Zebrafish, by Arpandhar (Own work) [CC BY-SA 4.0], via Wikimedia Commons.