Moselio Schaechter

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August 03, 2009

Playing the Light Organ Two Ways


The Hawaiian Bobtail Squid. Source.

by Elio

Deep within the oceans, sea animals and bioluminescent bacteria play symbiotic games. Fish, squid, and other animals that bring light to the darkness use it in their quest for food, their search for mates, or the avoidance of predators. This is not merely a curiosity, as seen by the simple fact that most animals living 2 km or more below the ocean surface are bioluminescent. One qualification: Not all of these bioluminescent animals depend on bacteria to generate light. Most do it all by themselves.

The usual way of thinking about these host-bacteria interactions has been straighforward: the host provides a site for the bacteria, the bacteria comply by making the light that is emitted from the animal. Actually, their interaction is not so simple. In the case of the well-studied Hawaiian Bobtail Squid, Euprymna scolopes, the host itself senses the light emitted by its symbionts, Vibrio fischeri— and not only with its eyes. Now, you ask, how does an animal perceive light other than by its eyes? It turns out that extra-ocular photodetectors are not uncommon among animals, this being but one example.

A recent paper from the McFall-Ngai lab sheds light (there, we said it!) on this story. First, some structure. The squid's light organ is not just a nondescript cavity where the bacteria thrive; it's a complex organ with some components analogous to the eye. Thus, it has a lens (with some of the same proteins as found in the lens of the eye), a reflective layer on the back, and even something of a "shutter" in the form of the squid's black ink sac. Next, some biochemistry. The light organ contains the visual pigment opsin and other proteins involved in optical transduction cascades. The latest news is that the light organ is itself photosensitive, with or without bacteria present. It responds electrophysiologically to light——but in a fashion distinct from that of the eye. (For those of you who speak electrophysiology: A characteristic rhabdomeric depolarization was observed in the electroretinographic spectra of the eyes, whereas the light-organ tissue responded with hyperpolarization.)


Colonies of bioluminescent bacteria
photographed by their own light. Source.

Animals that rely on bacterial symbionts for light production must be able to regulate their light emission. Since these squids use light for counter-illumination—that is, they achieve invisibility from below by matching their own light with that coming from above—too much or too little light wouldn't work. Little is known about how this is done, although there must be significant crosstalk between hosts and symbionts. For example, dark mutants of V. fisheri are rejected by juvenile squid and are not implanted in the light organ. This perception of light by the light organ may well be a mechanism for recognizing the luminescent-defective vibrios.

That the light organ of the squid has similar proteins as the eye suggests that it may be the product of evolutionary "tinkering," or "co-option," the assembly of existing components in new ways. The study of similarities and differences between the two organs promises (in the words of the authors) to provide insight both into conserved mechanisms of modulating and perceiving light and into the evolution of novelty. Well put.

Besides, these findings illuminate (there, we did it again) the intricate interactions that, given enough time, can evolve between closely-associated organisms. It makes good sense that the relationship would become fine-tuned, each partner sensitive to changes in the other. We've said this before, but there is something about symbioses that tickles the mind. Maybe it’s because, when it comes to complex phenomena, contemplating two genomes is better than one.

Tong, D., Rozas, N., Oakley, T., Mitchell, J., Colley, N., & McFall-Ngai, M. (2009). From the Cover: Evidence for light perception in a bioluminescent organ Proceedings of the National Academy of Sciences, 106 (24), 9836-9841 DOI: 10.1073/pnas.0904571106


The Hawaiian Bobtail Squid very neat looking picture!

Bioluminescence is fascinating and we can thank the Harvey's at Princeton years ago to start real serious work on it. There are some oddities of luminescence apart from bacterial luciferase. I remember Frank Johnson showing me a molecular non-enzymic version at Princeton produced by a Pacific Ocean jellyfish(do not remember species)that emitted points of light around its periphery by letting a few calcium ions into a vesicle containing an actifiable protein that released the photons. He followed the Harvey's in the Biology Department and was a very interesting guy.

I'm not surprised, Elio, that you chose this topic. After all, you are a "bright" fellow!

Yeah, I can pun, too. Sort of.

Luminescent symbioses remain a fascinating subject. I hope that you can induce one of the Famous Microbiology Quorum to write an essay on the Rhizobium-Legume symbiosis, which I think can further illuminate this topic (sorry), particularly the "cross-symbiont" communication conundrum!

By the way, I once heard a great story about the bioluminescent (and very large) pelagic tunicate, Pyrosoma atlantica. Here is some background:

First, bacterial bioluminescence never "blinks," as can eukaryotic-based bioluminescence phenomena When luminous prokaryotes appear to blink, it is because of the macrosymbiont's possession of something like a biological shutter mechanism, as in certain "flashlight fish." In any event, the enzymology of prokaryotic luciferase is quite different from that of eukaryotes, and relatively simple to tell apart.

Pyrosoma "blinks," is the way I have heard it, when you irritate the animal. Place a section of the tunicate in a blender, and it glows continually. Enzymatically, however, the activity seems to be characteristic of prokaryotic luciferases. Yet it blinks!

Perhaps the bacterial luciferase action is controlled by the animal partner in some biochemical fashion; the "blending" removes the host mediated control?

Anyway, I have never seen a good followup on this work...other than some discussion by Woody Hastings at Harvard and the Mackie and Bone ultrastructure paper. It's complicated by the fact that luminous bacteria are pretty common in the ocean, and the surface of the tunicate is sticky.

But I would love to know that more has been done!

By the way, Elio, there are some bioluminescent fungi, too...appealing to your mycophilia if not your mycophagia.

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