Play­ing the Light Or­gan Two Ways

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 Hawai­ian Bob­tail Squid. Source

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.

 

Ref­er­ence

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

 

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4 Comments
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17 years ago

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:
http://jellieszone.com/pyrosoma.htm
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.

R. G. E. Murray
17 years ago

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.

14 years ago

The Hawai­ian Bob­tail Squid very neat look­ing pic­ture!