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Study Challenges Evolutionary Relationship Between Flagellum and Type III Secretory System

Casey Luskin
Image credit: Illustra Media.

In an early intelligent design (ID) book, Darwin’s Black Box, biochemist Michael Behe argued that the bacterial flagellum is irreducibly complex. In case you haven’t been following ID, the flagellum is a micro-molecular machine — a propeller assembly driven by a rotary engine that propels bacteria toward food or a hospitable living environment. 

There are various types of flagella, but all function like a rotary engine made by humans, as found in some car and boat motors. Even non-ID scientists marvel at the complexity of these molecular machines. A new review in Journal of the American Chemical Society,Molecular Pumps and Motors,” states, “Biomolecular pumps and motors are, as is always the case in nature, complex and exquisitely crafted.” That is significant since “Biomolecular pumps and motors feature prominently in all living systems and are responsible for everything from DNA transcription and membrane transport to muscle expansion and contraction.” The review compares “man-made pumps and motors” to “their biological cousins” and notes that human technology is vastly inferior to biological machines: “the artificial molecular pumps and motors thus far developed by scientists are primitive compared to their natural counterparts.” 

An Irreducibly Complex System

Behe and like-minded scientists maintain that the flagellum requires a core number of subsystems and subcomponents to function, making it irreducibly complex and resistant to explanation by a stepwise mutational pathway. But not everyone agrees.

Critics of ID have often argued that another molecular machine, the type III secretory system (T3SS), may have served as a precursor to the flagellum. This argument even made its way into the 2005 Kitzmiller v. Dover decision. Biologist and ID-critic Kenneth Miller testified that “the 10 proteins in the type III system are almost a precise match for the corresponding 10 proteins in the base of the bacterial flagellum” and thereby could be a “precursor” to the flagellum. Following Miller, Judge Jones ruled that there is “a possible precursor to the bacterial flagellum, a subsystem that was fully functional, namely the Type–III Secretory System.” 

Not How Science Is Done

Science, however, isn’t decided by court rulings, and legal declarations on such scientific questions have significantly diminished value when new discoveries cast doubt on a court’s scientific claims. For example, a recent paper published in Cell by Jiaxing Tan et al., “Structural basis of assembly and torque transmission of the bacterial flagellar motor,” compared the structure of the flagellum to the T3SS and found that they have distinct differences which challenge such an evolutionary relationship:

It has been proposed that the bacterial flagellum is the evolutionary ancestor of T3SSs. Unlike the T3SS basal body, which is fixed in bacterial membranes, the MS ring, C ring, and rod of the flagellar motor rotate at high speeds when they function. … The overall structure of the [flagellar] motor-hook complex is larger and more complex than the T3SS basal body structure … However, FlgI does not exhibit sequence similarity with these T3SS components, indicating separate but convergent evolution of FlgI and the T3SS components for periplasmic binding. … The structure of the LP ring is significantly different from the C15-symmetric structure of the outer membrane-bound secretin of the bacterial T3SSs. … 

Although the flagellum has been proposed to be the evolutionary ancestor of T3SSs, the structure of the flagellar motor is significantly different from that of the T3SS basal body. The rod in the basal body of the Salmonella T3SS consists of two proteins, PrgJ and PrgI, and adopts a relatively simple helical structure. In contrast to the tight contacts of the T3SS rod with the secretin channel and the inner membrane ring, the flagellar rod has few contacts with the LP ring to facilitate its high-speed rotation and torque transmission. In addition, unlike the C24-symmetric inner membrane ring assembled by PrgH and PrgK in the Salmonella T3SS, the MS ring of the flagellar motor is composed of 34 FliF subunits with mixed internal symmetries. Therefore, the flagellar motor has evolved special structural elements for bacterial motility. [Emphasis added.]

These differences challenge the common evolutionary claim that the T3SS could have been “coopted” to build a flagellum. Indeed, if you carefully read the passage above, it says that “the flagellum has been proposed to be the evolutionary ancestor of T3SSs,” not that the T3SS was an “ancestor” of the flagellum. There are good reasons for why they did not claim the T3SS was ancestral to the flagellum, or that the two are derived from a similar ancestor, as I explained in 2015:

[I]t’s doubtful that the T3SS is useful at all in explaining the origin of the flagellum. The injectisome is found in a small subset of gram-negative bacteria that have a symbiotic or parasitic association with eukaryotes. Since eukaryotes evolved over a billion years after bacteria, this suggests that the injectisome arose after eukaryotes. However, flagella are found across the range of bacteria, and the need for chemotaxis and motility (i.e., using the flagellum to find food) precede the need for parasitism. In other words, we’d expect that the flagellum long predates the injectisome. And indeed, given the narrow distribution of injectisome-bearing bacteria, and the very wide distribution of bacteria with flagella, parsimony suggests the flagellum long predates injectisome rather than the reverse. As one paper observes:

“Based on patchy taxonomic distribution of the T3SS compared to that of the flagellum, widespread in bacterial phyla, previous phylogenetic analyses proposed that T3SS derived from a flagellar ancestor and spread through lateral gene transfers.”

(Sophie S. Abby and Eduardo P. C. Rocha, “An Evolutionary Analysis of the Type III Secretion System” (2012).)

Likewise, New Scientist reported:

“One fact in favour of the flagellum-first view is that bacteria would have needed propulsion before they needed T3SSs, which are used to attack cells that evolved later than bacteria. Also, flagella are found in a more diverse range of bacterial species than T3SSs. ‘The most parsimonious explanation is that the T3SS arose later,’ says biochemist Howard Ochman at the University of Arizona in Tucson.”

Now under normal evolutionary reasoning, one would take this kind of phylogenetic evidence to indicate that the flagellum long predates the T3SS, and that the T3SS is in no way a precursor (or closely related to a precursor) of the flagellum. 

The Last Bacterial Common Ancestor 

Indeed, a new phylogenetic study in Science, “A rooted phylogeny resolves early bacterial evolution,” proposes that the last bacterial common ancestor (LCBA) was “a free-living flagellated, rod-shaped double-membraned organism.” In other words, the widespread nature of flagellar genes across various types of bacteria suggest it is very ancient, perhaps even present at the root of all bacteria. As the paper explains: 

The inferred ancestral gene set for LBCA includes most components of the modern bacterial transcription, translation, and DNA replication systems. This gene set also includes an FtsZ-based cell division machinery and pathways for signal transduction, membrane transport, and secretion. Further, we identified proteins involved in bacterial phospholipid biosynthesis, suggesting that LBCA had bacterial-type ester-lipid membranes. We also identified most of the proteins required for flagella and pili synthesis and those for quorum sensing, suggesting that LBCA was motile. Given that bacterial genes are typically maintained by strong purifying selection, these findings imply that LBCA lived in an environment in which dispersal, chemotaxis, and surface attachment were advantageous. 

Because of these kinds of phylogenetic arguments for the widespread, ancient nature of flagella, a 2017 article in Nature Reviews Microbiology concluded that if anything, the flagellum is ancestral to the T3SS, not the other way around: 

Phylogenomic analyses indicate that T3SSs evolved from flagella and acquired the outer membrane secretin multiple times during evolution, arguing that ancestral T3SSs assembled from the inside-out in a similar manner to flagella, which do not have secretins. … Phylogenetic analysis of the core T3SS proteins revealed that the flagellar T3SS evolved first to transport extracellular components of the flagellum for assembly. NF‑T3SSs diverged from the flagellar T3SS, initially losing flagellum-specific proteins (particularly structural proteins that relate to the hook and rod), but gaining the inner membrane ring and inner rod components SctD and SctI, respectively.

But now this new paper in Cell has even challenged the view that the T3SS is descended from the flagellum, due to significant differences between the two structures. 

Another Challenge from the Critics

Another suggestion made by evolutionary critics of ID is that the flagellar motor shares structural homology with the rotary engine found in the ATP synthase molecular machine. However, the new Cell paper also finds that this comparison is suspect as there are important structural and functional differences between the flagellar motor and ATP synthase machines:

The flagellar motor is a rotary engine for torsional force transmission to enable bacterial motility. In contrast, the rotation of F/V-type ATPases, another type of natural rotational machinery, transmits torque force to induce conformational changes of the enzymatic domain for ATP synthesis or hydrolysis. The torque transmission mechanism from the rotary ring structure to the axial rod in the flagellar motor is different from that utilized by F/V-ATPases, in which the membrane-bound rotary ring forms a perpendicular surface attachment with the central stalk via salt bridges for planar-to-axial torsional force transmission. Thus, this work presents the structural basis for assembly and torque transmission of the flagellar motor and indicates the diversity of torque transmission mechanisms of natural rotary protein machineries.

These findings seemingly leave wide open questions about the evolutionary relationship of the flagellum and T3SS or other molecular machines. At the very least, it no longer appears possible that the T3SS is “a possible precursor to the bacterial flagellum.”