Surprisingly, there has been little discussion on a paper recently published in
PLOS Genetics. The paper is titled The Non-Flagellar Type III Secretion System Evolved from the Bacterial Flagellum and Diversified into Host-Cell Adapted Systems. What’s the big deal about this paper?
A number of ID critics involved in the origins debate have long believed that the bacterial flagellum evolved from the type III secretion system, or that the two systems share a common ancestral system that looked like an export system. For example, the Wikipedia article on the Evolution of flagella maintains that:
All currently known nonflagellar Type III transport systems serve the function of injecting toxin into eukaryotic cells. It is hypothesised that the flagellum evolved from the type three secretory system. For example, the bubonic plague bacterium Yersinia pestis has an organelle assembly very similar to a complex flagellum, except that is missing only a few flagellar mechanisms and functions, such as a needle to inject toxins into other cells. It is also a possibility that the flagellum could have evolved from a currently undiscovered system with similar flagellar traits or a currently extinct organelle/organism.
Back in the late 90s and early 2000s, you’d see ID critics arguing that the type III secretion system (TTSS) is a plausible precursor to the bacterial flagellum. At the time, some of the literature hinted towards another possibility: the TTSS may have evolved from the bacterial flagellum. This, then, was the response from ID proponents. When Gophna et al., 2003, published their phylogenies which suggested that the two systems shared a common ancestor, the debate took a different turn. It was now argued that the two systems had a common ancestor in the form of a protein export system. A poster on The Panda’s Thumb had this to say about the Gophna et al. paper:
Clue for the IDers: The TTSS appearing before the flagellum is not the only scenario that shatters your flawed and oversimplified arguments about the designed origins of the flagellum.
And in 2006, Nick Matzke said:
Back in 2003 I was about 55-45 for the idea that the flagellum came first, but Pallen’s parsimony argument and a few additional small points have moved me about 60-40 for the sister groups idea. There are several specific lines of investigation that could clear this up immensely.
(Note: Mark Pallen’s parsimony argument can be found here: Bioinformatics, genomics and evolution of non-flagellar type-III secretion systems: a Darwinian perspective, 2005)
Since 2003, the debate over the origin of the TTSS has been pretty split, with about half the papers saying that the TTSS descended from the flagellum, and the other half saying that the two systems share a common ancestor.
However, the recently published research provides strong evidence in favor of the hypothesis that the TTSS is derived from the bacterial flagellum. Let’s take a look at this a bit closer.
Here’s a quote from the paper:
A decade ago, several studies indicated one single phylogenetic split between the flagellum and the NF-T3SS [75], [79], [81], [82]. This is compatible with three different evolutionary scenarios. The two elements might have independent origins from an ancestral system, or one system might have adapted pre-existing structures from the other system for a new function [61], a process referred to as exaptation [83]. Understanding the details of the exaptation process requires an understanding of the direction of the evolutionary events. Current sequence databanks cover a much larger fraction of the prokaryotic world than ten years ago. Phylogenetic methods for dealing with multi-protein complexes have also been improved [84], [85], but these newer approaches have not yet been applied to infer the evolutionary history of T3SSs. The ongoing explosion of partially assembled genomes and metagenomes would also benefit from new tools for the detection and analysis of T3SSs from partial data. We have therefore produced such tools and applied them to genome data in order to determine the evolutionary origins and patterns of diversification of T3SSs.
The phylogenetic analyses of the TTSSs were done in this manner:
1. Maximum-likelihood phylogenetic reconstruction of the ATPase protein that is shared in the flagellum, TTSS, and F- and V- ATPases reveals that the TTSS nests within the flagellar clade. In this phylogeny, the F- and V- ATPases were used as the outgroup, thereby giving the tree a root. Moreover, this tree topology has a statistically significant bootstrap value (84%) in contrast to the two alternative topologies, with 7% and 9% bootstrap support.
2. This result was further supported by a phylogeny built from a larger dataset that included all curated systems.
Also, the study confirmed that the flagellar system has a much broader taxonomic distribution than the TTSS, again suggesting that the flagellar system is more ancient. The researchers also probed into the origin of the TTSS secretin, and found that TTSSs have acquired secretins independently at least 3 times.
Other comments
Some points in this paper that I would like to see improved in future studies:
1. The phylogeny that demonstrated that the TTSS is derived from the flagellum was only built from one protein group: the flagellar, TTSS, and F- and V- ATPases. It should be noted, however, that the TTSS ATPase, SctN, is the most highly conserved TTSS protein (Gophna et al., 2003). Because of the high level of sequence conservation in SctN, and its flagellar homolog, FliI, this protein should be expected to best portray the actual phylogenetic relationship of the flagellum and TTSS.
2. There is no mention of how the results offer a good response to Pallen’s parsimony argument (note: for those interested in the parsimony argument, I would urge you to look it up in Pallen et al.’s paper; in a future post, I may write up a critique of that parsimony argument based on this paper).
This paper is a substantial improvement over Gophna et al., 2003:
1. The study by Gophna et al., which concluded that the TTSS is ancient and did not descend directly from the flagellar system, used four different proteins to construct four different phylogenies. However, their trees were unrooted, which is not good. On the other hand, this study by Abby and Rocha rooted their phylogeny with an outgroup.
2. The bootstrap values for Gophna’s trees are not good, with the exception of one. The Abby and Rocha phylogeny has strong bootstrap support.
3. For phylogeny reconstruction, Gophna et al. used neighbor-joining, which is a distance-based method. Distance-based methods are among the least accurate phylogeny estimation methods, and can lead to incorrect results when lineages diverge at different rates (and it has been suggested that TTSS proteins have diverged faster relative to flagellar proteins). Meanwhile, Abby and Rocha employed maximum-likelihood, which is one of the most accurate phylogeny estimation methods out there.
In conclusion, this study significantly strengthens the hypothesis that the TTSS is derived from the flagellar system. Although we can still expect some of the non-specialists to continue arguing that the TTSS and flagellar system share a common, non-flagellar ancestor, anyone acquainted with the literature should not make such an argument. There is one more important point to make here. If the TTSS descended from the flagellum, then about half of the flagellar proteins lack any precursor homologs. Finally, since the TTSS does not share a common, non-flagellar ancestor with the bacterial flagellum, the TTSS is not evidence that the flagellar system evolved from a primitive secretion system.
Thoughts?
Referrences
1. Abby SS, Rocha EPC (2012) The Non-Flagellar Type III Secretion System Evolved from the Bacterial Flagellum and Diversified into Host-Cell Adapted Systems. PLoS Genet 8(9): e1002983. doi:10.1371/journal.pgen.1002983.
2. Gophna, U., Ron, E., Graur, D., 2003. Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. Gene 312,151-163.
3. Pallen MJ, Beatson SA, Bailey CM., 2005. Bioinformatics, genomics and evolution of non-flagellar type-III secretion systems: a Darwinian perspective. FEMS Microbiol Rev. 29(2):201-29.
*Note: technically, I should be using the term NF-T3SS to indicate which TTSS I’m referring to. In this post, though, read TTSS as synonymous with NF-T3SS.
Edited by Genomicus, : No reason given.
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