Evil polyps enslave innocent algae using light


Imagine you’re swimming in nice, warm water, happily making your own food without a care in the world (other than zooplankton). You just need to store up enough starch before nightfall to hold you through the night so you can quit swimming, absorb your flagella, and wait for the sun’s return. You see a green light below, and you swim toward it. You can’t help yourself; your phototactic machinery is hardwired to respond.

Next thing you know, you’re captured by a giant, tentacled polyp. You look for a way out, but there is none. You’re stuck there for the rest of your life, forced to work and have the food you produce stolen by your coral overlord. Resigned to your fate, you absorb your flagella and get down to photosynthesizing.

Aihara et al. 2019 Fig. 2A

Figure 2A from Aihara et al. 2019. the coral Echinophyllia aspera and its algal captives under natural light conditions (Scale bar, 1 cm.).

Corals rely on algal symbionts to provide sugar and amino acids. Loss of the symbionts, known as bleaching, is often fatal for the corals. The right kinds of algae, though, are not common around reefs, so the corals need a way to attract them. Amazingly, how they do this isn’t exactly known. The chief suspects are chemical attraction and green fluorescence.

A team of researchers from Japan and Australia has convinced me that green fluorescence is at least part of the answer. In a new paper in the Proceedings of the National Academy of Sciences, Yusuke Aihara and colleagues show that the dinoflagellate Symbiodinium is attracted to green fluorescence produced by coral.

The corals produce a protein, green fluorescent protein (GFP), that emits green light when it’s exposed to purple-blue light. In three separate experiments, Aihara and colleagues tested whether Symbiodinium was attracted to the fluorescence. Two of the experiments used a green fluorescent dye with a similar emission to GFP, one in the lab and one in the wild. In both cases, the algae were more attracted to the dye than a non-fluorescent control. A separate experiment used live algae, with dead algae as a control. Both the live and dead fragments were coated with resin plastic to prevent chemotaxis:

The video above was shot under blue LED light. The live coral is on the right, dead on the left, and the algae are initially well mixed.

The combination of experiments seems to account for all the possibilities. The live coral experiment shows that the algae are attracted to the coral when they’re fluorescing, but it doesn’t completely rule out that it could be something other than the fluorescence attracting them, and it doesn’t show that the attraction to GFP works in natural conditions. The other two experiments neatly dispose with both of these possibilities, showing that the algae are attracted to the fluorescence per se, and that this attraction occurs even in full sunlight.

How are they attracted to the relatively weak fluorescence in the face of much stronger direct sunlight? The authors address this in the Discussion:

Free-living Symbiodinium potentially sense at least two different phototactic signals from opposite directions; one is the light signal from the sun, and the other is the fluorescent signal from benthic corals. Thus, the attraction of Symbiodinium to corals occurs only if the positive phototaxis toward the fluorescent signal is dominant.

A previous experiment showed that the algae are specifically interested in the green part of the light spectrum:

Hollingsworth et al. Fig. 1

Figure 1 from Hollingsworth et al. 2005. Motile algal cultures exposed to a visible light spectrum after 15 min exposure. The dark smudge in the green portion of the spectrum is a dense concentration of motile algae.

As the water gets deeper, the light that penetrates loses the longest wavelengths first, meaning that it is getting bluer as it gets darker. At some depth, there will be more green light from the fluorescence below (GFP is excited by blue-violet light, the last to be lost) than from the sunlight above:

It is therefore likely that the light intensity required for the attraction of Symbiodinium by green fluorescence differs with light spectra and depth. Because blue light penetrates seawater to a depth of ∼50 m, the attraction of Symbiodinium by green fluorescence potentially occurs in both shallow and deep water.

There is even some evidence that the corals increase the amount of GFP they produce when they are most in need of the algae:

GFP-associated fluorescence is higher in larvae and juvenile coral polyps that lack symbionts compared with those that have symbionts, again suggesting a role for green fluorescence in attracting symbionts at this crucial life stage (38). The survival of corals affected by stress, such as the loss of symbionts after exposure to high temperature, might also rely on recruiting symbionts from the environment. This hypothesis is consistent with results showing that GFP-associated fluorescence is higher in bleached corals than in nonbleached ones (39).

The experiments don’t rule out that some other factor (such as chemotaxis) could attract algae to the corals in addition to fluorescence, but they show pretty convincingly that fluorescence is at least sufficient to attract the algae.

So the corals would seem to have hijacked the algae’s natural attraction to green light and used it as a lure, even to the point of adjusting the expression of the gene that produces GFP in a way that makes algal capture most likely when it is most needed. It’s also not out of the question that the algae themselves might have adapted to optimize their response; in spite of my hysterical headline, it’s not all bad for the algae. They get a (relatively) safe place to live, protected from the hazards of voracious zooplankton, if not from the occasional parrotfish.

 

Stable links:

Aihara Y, Maruyama S, Baird AH, Iguchi A, Takahashi S, Minagawa J. 2019 Green fluorescence from cnidarian hosts attracts symbiotic algae. Proc. Natl. Acad. Sci. doi:10.1073/pnas.1812257116

Hollingsworth LL, Kinzie RA, Lewis TD, Krupp DA, Leong JAC. 2005 Phototaxis of motile zooxanthellae to green light may facilitate symbiont capture by coral larvae. Coral Reefs 24, 523. doi:10.1007/s00338-005-0063-8

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