The Sinister Type III Secretory System?
By Mike Gene (
The type III secretory system (TTSS) is a subsystem of the bacterial flagellum that appears to have been spawned from the flagellum sometime after the appearance of eukaryotes. Most studies of the TTSS have focused on pathogenic bacteria, which is understandable given that such work is most likely to be funded. Yet this skewed sampling has led many to equate the TTSS system as a disease-causing device. For example, the Bubonic Plague was caused by a species of bacteria that uses the TTSS.
The fact that the TTSS appears to be a molecular machine which causes disease has not gone unnoticed by many critics and proponents of design. And while detecting design is not dependent on the designed thing serving a benevolent or sinister purpose, proponents of design typically express some level of discomfort about something that looks like a designed bio-weapon and opponents of design typically exploit this concern for rhetorical purposes.
But is it really accurate to think of the TTSS as a designed bio-weapon? It’s important to realize that when I tentatively infer design for something like the flagellum in E. coli, I am not inferring that the E. coli flagellum that we study in the lab was the very thing that was designed. On the contrary, I envision an originally designed flagellum (or set of similar flagella) that have since experienced a few billion years of evolution. That is, the E. coli flagellum is a descendent of design, not the actual design itself.
When it comes to the TTSS system, the same logic would hold. If I scored the TTSS as designed, I would not score the TTSS from Yersinia (the agent of Bubonic Plague) as the thing that was designed. It would simply be a descendent of some ancestral version of a TTSS.
But why design the TTSS? If it commonly causes disease, was the design objective to create disease among multicellular eukaryotes? After all, the TTSS usually depends on contact with the host cells to initiate the process of TTSS construction and transport of proteins that manipulate the host cellular processes.
We must remember that from a biological perspective, disease by bacteria is essentially a form of parasitism. And parasitism, in turn, is a form of symbiosis, where two or more organisms exist in some form of direct relationship. And there is a wide range of symbiotic relationships, from mutualistic associations where both members benefit from the relationship to parasitic associations where one member benefits at the expense of the other. Might the TTSS be a machine to establish symbiotic connections between the very different worlds of the bacteria and eukaryotes?
A long recognized example of a mutualistic relationship between bacteria and plants is the symbiosis between Rhizobium and legumes. This is an association that leads to rather dramatic morphological and biochemical changes in the plant root and the bacterial cells. It is a fascinating example of evolution (to be explored later), where the bacteria fix nitrogen and provide it to the plant and the plant, in return, provides nutrients for the bacteria. The relationship is of great commercial interest. And it is mediated by the TTSS.
Might this be the tip of the iceberg? It was recently discovered that the TTSS also mediates an intimate endosymbiotic relationship between a gram-negative bacterium and rice weevils. [1] In this relationship, the bacteria provide various vitamins to the weevil to increase mitochondrial enzymatic activity which, in turn, greatly enhances the flight ability of adults. What is of interest is similar bacteria are widespread among arthropods and known alter their reproduction, raising the possibility that bacteria have a played in a key role in arthropod evolution. Might such relationships involve other bacteria and phyla?
The TTSS has indeed played a significant role in plant and arthropod evolution and I would predict that such examples will accumulate over time. If the TTSS evolved from a designed flagellum, this raises the issue of front-loaded evolution. Future essays will explore this in more depth.
1. Dale C, Plague GR, Wang B, Ochman H, Moran NA. 2002. Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc Natl Acad Sci U S A. 99(19): 12397-402.