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20 Years of Challenging Evolution: Is the Bacterial Flagellum Irreducibly Complex?

Thu, Sep. 18, 2014 Posted: 09:20 PM

About forty years ago biologists discovered that some bacteria swim by means of a rotating flagellum, which is a long whip-like propellor connected to a rotary engine that is situated within the cell membrane. About twenty years after this discovery biochemist Michael Behe began to argue that the bacterial flagellum and many other molcular machines within living cells exhibit the property of "irreducible complexity," which implied that the likelihood of their origin by means of an unguided material process is beyond reasonable belief. What has become of this argument in the last twenty years? Has the overall trajectory of research supported or eroded Behe's case for the "irreducible complexity" of molecular machines like the bacterial flagellum?

In his book Darwin's Black Box (1996) Behe explained that irreducibly complex systems could not have arisen by a gradual step-by-step neo-Darwinian evolutionary process.

The flagellum is a long, hairlike filament embedded in the cell membrane. The external filament consists of a single type of protein, called "flagellin." The flagellin filament is the paddle surface that contacts the the liquid during swimming. At the end of the flagellin filament near the surface of the cell, there is a bulge in the thickness of the flagellum. It is here that the filament attaches to the rotor drive. The attachment material is comprised of something called "hook protein." The filament of a bacterial flagellum, unlike a cilium, contains no motor protein; if it is broken off, the filament just floats stiffly in the water. Therefore the motor that rotates the filament-propellor must be located somewhere else. Experiments have demonstrated that it is located at the base of the flagellum, where electron microscopy shows several ring structures occur. (p. 70-72)

Behe's 1996 conclusion:

In summary, as biochemists have begun to examine apparently simple structures like cilia and flagella, they have discovered staggering complexity, with dozens or even hundreds of precisely tailored parts. It is very likely that many of the parts we have not considered here are required for any cilium to function in a cell. As the number of required parts increases, the difficulty of gradually putting the system together skyrockets, and the likelihood of indirect scenarios plummets. Darwin looks more and more forlorn. New research on the roles of the auxiliary proteins cannot simplify the irreducibly complex syetem. The intransigence of the problem cannot be alleviated; it will only get worse. Darwinian theory has given no explanation for the cilium or flagellum. The overwhelming complexity of the swimming systems push us to think it may never give an explanation. (p. 73)

What's become of this argument in the last two decades? Some say "irreducible complexity" has been refuted. Here's a list of essays that show that the argument is still very strong. In some respects the "irreducible complexity" argument against neo-Darwinism and for intelligent design is more robust than every before. We will focus on just the case of the bacterial flagellum to help make this point, rather than chase down the thousands of other molecular machines that are also arguably irreducibly complex. We shall take this up in a rational order, rather than historical-chronological order.

1. The Assembly Mechanisms to Form a Flagellum are More Irreducibly Complex than the Flagellum

How does a bacterium alive today construct its own flagellum? In the 2002 Illustra documentary Unlocking the Mystery of Life, Scott Minnich made the case that the assembly instructions for building a flagellum are even more irreducibly complex than the outboard motor structure itself. An August 2013 paper in PNAS announced discoveries that show an amazing sequential assembly routine that is necessary for flagellum construction.

In this study, we genetically trapped intermediates in flagellar assembly and determined the 3D structures of the intermediates to 4-nm resolution by cryoelectron tomography. We provide structural evidence that secretion of rod substrates triggers remodeling of the central channel in the flagellar secretion apparatus from a closed to an open conformation. This open channel then serves as both a gateway and a template for flagellar rod assembly. The individual proteins assemble sequentially to form a modular rod. The hook cap initiates hook assembly on completion of the rod, and the filament cap facilitates filament assembly after formation of the mature hook.

Here's how an ENV essay explains the significance of this 2013 publication.

The 12 authors from 5 American universities don't seem to have much use for evolutionary theory. They never mention it. Instead, they call the flagellum a "sophisticated self-assembling molecular machine" and, twice, "an intricate molecular machine."

This 2013 PNAS article helps confirm the sequential nature of construction that Minnich described in the 2002 film Unlocking the Mystery of Life:

[Minnich] Even if you concede you had all the parts necessary to build one of these machines, that's only part of the problem. Maybe even more complex -- I think more complex -- is the assembly instructions. That is never addressed by opponents of the irreducible complexity argument.

[Narrator] Studies of the bacterial motor have, indeed, an even deeper level of complexity. For its construction not only requires specific parts, but also a precise sequence of instructions for assembly.

[Minnich] You've got to make things at the right time. You've got to make the right number of components. You've got to assemble them in a sequential manner. You've got to be able to tell if you've assembled it properly so that you don't waste energy building a structure that's not going to be functional....

You build this structure from the inside out. You're counting the number of components in a ring structure or the stator, and once that's assembled, there's feedback that says, "OK, no more of that"; now, a rod is added; a ring is added; another rod is added; the U-joint [hook] is added. Once the U-joint is add a certain size, and a certain degree of bend, about a quarter turn, that's shut off, and then you start adding components for the propeller. These are all made in a precise sequence, just like you would build a building.

In this same 2002 film Paul Nelson observes that the construction of an irreducibly complex machine such as the flagellum requires the work of other machines. In turn, those machines require yet other machines for their assembly. This suggests that the whole assembly apparatus for such molecular machines is itself irreducibly complex. Jonathan Wells stated the situation provocatively in the 2002 Illustra documentary: "what we have here is irreducible complexity all the way down."

Although the 2013 PNAS article does not use the term irreducibly complexity, their description matches Minnich's 2002 language, which strengthened Behe's original arugment. Read further analysis of the 2013 dicoveries of flagellar assembly here to further appreciate how Minnich's extension of Behe's argument has been significantly strengthened by these recent findings.

2. The Cell Has a Complex Feedback System that Determines How Long to Grow each Flagellum

How does a bacterium store and process the information needed to determine the length of a flagellum in a particular bacterial species? Although we still have much to learn about this, in 2012 discoveries pointed to sophisticated feedback controls. An ENV essay explains:

Two scientists at UC San Francisco looked into the question recently in Science, "How Cells Know the Size of Their Organelles." Chan and Marshall discussed several ways cells can monitor the size of their construction sites. Here's a little something that makes you say "wow," pointing to the sophisticated controls that are at work:

In the biflagellate green alga Chlamydomonas, when one flagellum is severed, during its regeneration the other, intact flagellum shortens until the two flagella reach equal lengths, at which point they resume growth together. This equalization of lengths seems to indicate that the cell "knows" how long both its flagella are. (Emphasis added.)

The tip of a flagellum is way out there, extending into the outside environment. What brings information from that distant point back to the nucleus, where the parts are constructed? The cell can't see it; it has to get chemical messages from that distant frontier somehow without [what we might call] telegraph lines.

You might recall that in the film Unlocking the Mystery of Life, Scott Minnich said that the cell has a signal transduction system that gets feedback from the environment. That was a decade ago and scientists are still trying to figure out how it works.

Chan and Marshall list five methods a cell could use to monitor and control organelle size. "Reporter" molecules might, for instance, be responsive to time, density, structure or some other aspect of the organelle's growing size or shape. Eukaryotic [i.e., non-bacterial] flagella are built by a complex system called "intraflagellar transport" (IFT). Consider this amazing fact: construction parts are delivered to the tip of a flagellum by tiny carts riding along tracks! These carts travel out to the tip and deliver the cargo, like ore carts in a mineshaft....

If you know of any observations that show a blind, aimless process capable of producing a finely tuned mechanism that functions like an outboard motor, using sensory feedback from the environment, be sure to let the world know. Publish your results! Besides winning plaudits in precincts of biology, you'll likely revolutionize teaching methods in the engineering and architecture departments as well. Read more.

3. Flagellar Filament Cap (at the Flagellum's End): An Amazingly Dynamic Protein Structure

Here's how an ENV essay introduces the topic, which has advanced remarkably in the past fifteen years:

Imagine you are an archaeologist surveying the remains of a formerly technologically advanced civilization. You stumble across the device depicted in the figure above. With its pentagon-shaped plate and its carefully crafted leg-like extensions, it looks like it came from some sort of machine. Immediately, you intuitively infer that the device was designed intentionally, for a purpose. This isn't the kind of device that is typically created by forces of nature such as wind and erosion.

You may be wondering what the device in the figure is, or what machine it forms a part of. The measurements indicate that, whatever it is, it is certainly extremely small. The figure, which was excerpted from Maki-Yonekura et al. (2003), in fact reveals a reconstructed three-dimensional image of the flagellar filament capping protein (also known as FliD). Here it is in context (credit for animations goes to Keiichi Namba et al. of the ERATO Protonic NanoMachine Project):

The activity of the capping protein of the bacterial flagellar filament -- which serves as a rotary promoter for self-assembly of flagellin monomers -- has been described as "one of the most dynamic movements in protein structures" (Yonekura et al., 2000).

FliD is in fact critical to filament assembly. Without the presence of FliD, the flagellin monomers are lost (Kim et al., 1999). As one paper has explained, "A FliD-deficient mutant becomes non-motile because it lacks flagellar filaments and leaks flagellin monomer out into the medium" (Ikeda et al., 1996). Indeed, FliD is crucial for proper assembly of the flagellin proteins, as shown in the animation (right). What is even more interesting still is that FliD presently has no known homologues in non-flagellar systems.

How, then does the capping protein work, and why is it so essential? Read more.

4. Attempts at Directly Refuting the Irreducibly Complexity of the Flagellum have Failed

Here's an essay about the latest failed attempt to refute Behe's argument about the bacterial flagellum. It begins:

I've been reading the recently published book Microbes and Evolution: The World that Darwin Never Saw, which combines my two primary areas of interest: microbiology and evolution. Chapter 38 of the book is written by Kelly Hughes and David Blair of the University of Utah, two of the world's leading experts on bacterial flagellar assembly. Having followed the work of Kelly Hughes and his colleagues for a few years, I hold their work in the highest regard. I myself have a deep fascination with the subject of bacterial gene expression. I was intrigued, therefore, when I discovered the title of Hughes and Blair's chapter: "Irreducible Complexity? Not!"

Read why (the reasons are a bit technical) the following conclusion about the work of Hughes and Blair is appropriate:

To conclude, the claim of Hughes and Blair to have refuted Behe on the bacterial flagellum is unfounded. Although there are sub-components of the flagellum that are indeed dispensable for assembly and motility, there are numerous subsystems within the flagellum that require multiple coordinated mutations [in order to originate by a Darwinian process of mutation and natural selection]. The flagellar motor is not the kind of structure that one can at all readily envision being produced in Darwinian step-wise fashion.

So, after 20 years, the argument for the irreducible complexity of the bacterial flagellum is in great shape. For more related reading, see Responding to Darwinists Claiming to Have Explained Away the Challenge of Irreducible Complexity.

Mike Keas