Tuesday, November 27, 2007

Quorum Sensing or Diffusion Sensing?

I'd like to call attention to an interesting couple of posts at one of my favorite science blogs, RRResearch. I find them interesting because they highlight two opposing views of the function of small signaling molecules (autoinducers). One view (Quorum Sensing) suggests that microbes secrete these molecules in order to estimate population density and predict the utility of investing in secreting molecules that can be used by the whole population. In this view, secreting shared molecules is an inherently cooperative behavior, and as such is exploitable by cheating.

Rosie Redfield has suggested an alternative explanation: diffusion sensing. Her paper in Trends in Microbiology hypothesized that "bacteria instead secrete and detect autoinducers as a method of determining whether the benefits of secreting more expensive effector molecules will limited by diffusion and mixing." This is an inherently selfish behavior because "it would be a waste of resources to secrete degradative enzymes such as proteases if they are going to immediately wash away."

The whole issue hearkens back to George Williams classic, Adaptation and Natural Selection. If that book is to be summarized in one sentence, it might be "Thou Shalt Not Invoke Group Level Adaptations When Individual Level Adaptations Will Suffice!" That is, don't claim an adaptation benefits a group of organisms when plausible explanations invoking benefits to individuals are available. By this rule, quorum sensing might be a valid explanation for autoinducer secretion, but only after diffusion sensing explanations are ruled out.

I share Rosies' frustrations. Every time someone tells me about this wonderful new experiment showing that bacteria cooperate (which, in some cases, they no doubt do), I always groan and ask if they read Rosie's paper. Invariably they haven't.

The series of posts is interesting in another light. It shows the process of science in action, which is usually an opaque process to most people. Here we have two opposing "schools of thought" arguing about the proper way to interpret ambiguous data. In the long run, it will be the hypothesis that best explains the data that "wins". In this case, the debate plays out in the blogosphere and not behind the august pages of Nature (available by subscription only).

Update: I missed this earlier, but Ford Denison of This Week in Evolution wrote a nice post about the original Diggle et al. Nature paper here.

Photo: Vibrio fischeri growth on Petri dishes after incubation in nano CuO suspension. V. fischeri is a putative case of quorum sensing. Photo from KBFI.


  1. Even worse. I've made quite a few people read the paper and even having done so, most people seem to almost willfully miss the point that the diffusion sensing hypothesis negates the need to invoke group benefits.

    Very frustrating

  2. A key assumption of the diffusion hypothesis is that a single cell can make enough extracellular enzyme to benefit itself, i.e. that cells find themselves in small enclosed spaces with limited diffusion fairly often. Has anyone looked at this question quantitatively? Another assumption (probably true) is that it's cheaper to make the quorum/diffusion probe to use the extracellular enzyme itself as the probe.

  3. rford,

    I am not sure that an enclosed space is a necessary condition. The viscosity of aqueous solutions is quite high at micro-scales. Since we are talking about relatively large molecules, it is possible that they might not diffuse away very quickly even in relatively open environments. If I recall my fluid dynamics correctly, diffusion can also be quite low on boundries, such as the surface of particles.

    I agree that a key assumption of the hypothesis is that a single cell can make enough enzyme to benefit itself. My question is: why is the default assumption that they can't?

  4. Rosie cites this paper as evidence for the hypothesis that cells can make sufficient enzymes to benefit themselves.

    Full quote from her paper, "For example, in laboratory cultures of the soil bacterium Bacillus subtilis, autoinducers reach inducing concentrations at culture densities <10^8 cells ml-1 [17], implying that each cell can fill a volume of 10^4 μm3 with an activating concentration of inducer."

    I'm sure a lit search will turn up further examples.

  5. Thanks, Andrew and John. Toby Kiers and I are working on an article for Annual Review of Ecology etc. on the rhizosphere mutualisms. For some microbial activities that happen to benefit plants (and, indirectly, other microbes) it's easy to see potential benefits to individual microbial cells, but quorum-sensing seemed to indicate an important role for kin selection as well. Now we'll have to re-evaluate some of those examples.

  6. Ford, that should be an interesting article. Keep me posted on it!

  7. John, thanks for the boost.

    Rford, there's a nice paper from Ken Bayles lab (Shompole et al. 2003 Mol. Micro. 49: 919-927) showing that single Staph aureus cells use autoinducers to detect that they are in an intracellular endosome and to induce expression of the genes that get them out into the cytoplasm.