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Berkeley MCELLBI 140 - From The Origin of Species to the origin of bacterial flagella

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© 2006 Nature Publishing Group Almost all microbiologists are familiar with either the bacterial flagellum (BOX 1) or type III secretion systems (T3SS), but most would have been surprised to hear these subjects feature prominently in a United States courtroom. Yet that is precisely what happened last year in the Kitzmiller versus Dover trial in Pennsylvania, where the term ‘flagellum’ and its cognates appeared 385 times in the transcripts of the 6-week trial. These topics were brought to the attention of the public, as the trial judge heard quota-tions from eminent bacteriologists, such as David DeRosier, Carl Woese, Richard Lenski, Richard Losick and Lucy Shapiro. The chief findings of the trial judge, John E. Jones III, can be summarized by a few sentences: he found it “…abundantly clear that the board’s ‘intelligent design’ (ID) policy violates the establishment clause. In making this determination, we have addressed the seminal question of whether ID is science. We have concluded that it is not, and moreover that ID cannot uncouple itself from its creationist, and thus religious, antecedents.” In short, the ‘Bacterial Flagellum Trial’ (as one of the defence lawyers called it) estab-lished that the teaching of ID in American state schools was unconstitutional.The myth of irreducible complexityBut why was microbiology discussed in this court case? The answer lies in the fact that members of the ID movement (including two witnesses for the defence in the Dover trial, Michael Behe and Scott Minnich) cite the bacterial flagellum as an example of an irreducibly complex system. This complexity, they argue, could not have arisen through gradual variation and natural selection, which were proposed as the mechanism of evolution in Darwin’s The Origin of Species (BOX 2). At the heart of the ID argument is the supposition that some biological systems are so complex that they can only function when all of their components are present, so that the system could not have evolved from a simpler assemblage that did not contain the full machinery — essentially a modern re-working of the old creationist argument ‘what good is half a wing?’Kenneth Miller, who appeared as a witness for the plaintiffs, elaborated, in non-technical terms, some of the arguments against the notion that the flagellum is irreducibly complex (see Further informa-tion for links to trial material); he and others have also done so in print1,2. Crucially, Miller pointed out that the flagellum is modular, in that the T3SS that is responsible for flagellar protein export constitutes a functionally intact subsystem capable of performing a useful function (protein secretion) in the absence of the rest of the flagellar apparatus. However, there are additional arguments, which we elaborate below, in favour of viewing bacterial flagella as evolved — rather than designed — entities.Beyond typologyAs the great evolutionist Ernst Mayr noted, one of Darwin’s greatest achievements was to abolish typological or essentialist think-ing from biology; instead, the emphasis in biology is on variation and individuality3. Therefore, when discussing flagellar evolu-tion it is important to appreciate that there is no such thing as ‘the’ bacterial flagellum. Instead, there are myriad different bacterial flagella, showing extensive variation in form and function. The most well-studied bacte-rial flagellar system is that of Salmonella enterica serovar Typhimurium (Salmonella typhimurium) (BOX 1). However, in Gram-positive bacteria, flagella lack P- and L-rings4, and in spirochaetes the flagellar filaments rotate inside the periplasm5. Some flagella rotate using proton-motive force, others depend on a sodium-ion gradient6,7. In Sinorhizobium meliloti and Rhodobacter sphaeroides, the flagellum rotates unidirectionally, with a fast, slow or stop mechanism, whereas in S. typhimurium reversals in the direction of flagellar rotation are used to re-orientate the cell8,9. Flagellar filaments vary in their physical properties: some show right-handed helical packing, others left-handed; some are flexible, others rigid; some are straight, others curly10; some undergo post-translational modifications such as glycosylation or methylation, others do not11,12. In Escherichia coli alone there are over forty antigenically distinct flagellins, with good evidence that variation is driven by diversifying natural selection13. Indeed, flagellins in general provide a perfect illus-tration of Darwin’s dictum14 that “nature is prodigal in variety, though niggard in innovation”, in that the surface-exposed domains are highly variable, ranging in length from effectively zero to 800 residues, yet the peripheral domains that mediate inter-subunit interactions are highly con-served15. Furthermore, some systems deploy a single flagellin, whereas others, like the S. typhimurium model system, exploit two different flagellins, but never in the same filament. In other exceptional cases, up to six different flagellins are incorporated into a single flagellum16.Many new flagellar systems have been discovered through genome sequencing — a trend that is likely to increase with time. For example, over three hundred flagel-lin sequences were obtained in a single sequencing project that focused on samples from the Sargasso Sea17. By even the most conservative estimate, there must therefore be thousands of different bacterial flagellar systems, perhaps even millions. Therefore, there is no point discussing the creation or ID of ‘the’ bacterial flagellum. Instead, one is faced with two options: either there were thousands or even millions of individual creation events, which strains Occam’s razor to breaking point, or one has to accept that all the highly diverse contemporary flagel-lar systems have evolved from a common ancestor.Another line of evidence suggesting that flagellar systems are subject to the same evolutionary forces as other biological enti-ties comes from the discovery of vestigial SCIENCE AND SOCIETYFrom The Origin of Species to the origin of bacterial flagellaMark J. Pallen and Nicholas J. MatzkeAbstract | In the recent Dover trial, and elsewhere, the ‘Intelligent Design’ movement has championed the bacterial flagellum as an irreducibly complex system that, it is claimed, could not have evolved through natural selection. Here we explore the arguments in favour of viewing bacterial flagella as evolved, rather than


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Berkeley MCELLBI 140 - From The Origin of Species to the origin of bacterial flagella

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