In chemical ecology, the devil--or the coral settlement cue--is in the details

This week we provide a quick overview of a suite of compounds found in Nature to highlight a central tenet in chemical ecology.

Small differences in the structures of molecules can result in vastly different bioactivities.  To quickly illustrate this concept, let's take a look at two familiar molecules: Splenda, many a dieter's favorite sweetener, and good ole sucrose, the calorie-full sugar in fruit and other foods. We can see that the only difference between these structures is the presence of three chloride atoms in place of hydroxyl (OH) groups in Splenda's structure. Those three halide atoms make the difference between your no-calorie drink and a sugar-laden treat.

Small differences in chemical structure make a big difference. For splenda and sucrose the difference is in three highlighted chloride atoms... and whether you lose weight or not! ;)

Small differences in chemical structure make a big difference. For splenda and sucrose the difference is in three highlighted chloride atoms... and whether you lose weight or not! ;)

Today's focus will be three different molecules that all have halide (e.g. chloride, bromide) atoms and planar (i.e. flat) rings of carbon atoms. Otherwise there isn't too much linking them. So enjoy each of these nuggets of chemical ecology like you would a fine cheese: Savor, enjoy and share with a friend.

The first compound comes from the paper that got me thinking about this concept to begin with. The paper was published in Nature Chemical Biology in 2017 and is largely the work of scientists in San Diego at the Scripps Institution of Oceangraphy. In this paper they report conclusive evidence that a very common metabolite found in marine sponges is actually produced by the bacterial symbionts that inhabit the sponges, not the sponge itself. This metabolite is a polybrominated diphenyl ether (PBDE). There are a range of highly similar compounds in this same class of PBDEs that are made by the bacteria and deposited in the sponge tissue. The structure of one of the common PBDEs found in sponges is right here:

Polybrominated diphenyl ethers are common marine metabolites and are made by bacteria that live in sponges. 

Polybrominated diphenyl ethers are common marine metabolites and are made by bacteria that live in sponges. 

Here are a few fun facts :

  • PDBEs can make up to 12% (!) of the dry weight of marine sponges within the family Dysideidae.
  • Despite its serious presence in sponge tissue, the biological activity of these compounds in the context of the sponge-bacterial symbiosis is not clear. Why do the bacteria make so much? 
  • PDBEs are abundant in marine ecosystems and are found across all trophic levels, from whales to bacteria. This is because PDBEs bioaccumulate: they are not easily broken down in living tissues and persist over the lifetime of many animals (including us!)

Interestingly, PDBEs look a lot like some of the nastiest human-made chemicals we know of! This brings us back to a class of compounds that we've discussed before on this blog: polychlorinated biphenyls (PCBs).

Shown here is the polychlorinated biphenyl PCB 156, which was Produced by many chemical companies until the 70s. In the 1970s, public awareness and expert knowledge about the harm caused by PCBs started to rise. The Toxic Substances Control Act banned the production of PCBs in the U.S. in 1978 thanks, Epa!

Shown here is the polychlorinated biphenyl PCB 156, which was Produced by many chemical companies until the 70s. In the 1970s, public awareness and expert knowledge about the harm caused by PCBs started to rise. The Toxic Substances Control Act banned the production of PCBs in the U.S. in 1978

thanks, Epa!

Previously at Chemical Intuition we've discussed PCBs in the context of how these and other persistent industrial chemicals have impacted the evolution of fish in highly polluted waters. That story focused on the brilliance of evolution to solve problems of survival in a hostile world. Let's focus on the chemistry of PCBs--why were they so popular with industry in the first place? What makes them bioaccumulate? Besides fish, what other organisms are affected by these compounds?

PCBs--why so popular?

Here are some physical characteristics of PCBs that help explain their popularity:

  • low electrical conductivity/insulating
  • non-flammable
  • chemical stability (i.e. these types of molecules don't easily break down when exposed to air, high temperatures)

These chemical and physical characteristics made PCBs good chemicals to help make:

  • electrical stuff, especially capacitors and transformers
  • paints and dyes
  • lighting fixtures: PCBs are part of the fluorescent light ballasts that make working inside in most office buildings such a natural-lighting joy :S
  • rubber and other bendy plastics

What makes them bioaccumulate?

The chemical stability of PCBs makes these chemicals difficult for our bodies to eliminate. And the chemical stability and lack of a biological route of degradation means that PCBs persist in the environment for very long periods of time. The half-life of elimination (i.e. the amount of time it takes for half of an initial amount to "go away" through direct elimination or degradation) of PCBs in the adult human body has been calculated to be around 10-15 years. That's a very long time if you compare it to how fast the human body can deal with alcohol (hours) or THC (a few days).

What organisms are affected by these compounds?

According to the EPA, PCBs have a wide-range of negative health effects on organisms, from fish to humans, at a range of doses, including chronic (small doses over a long period of time) and acute (high dose over a short period of time) doses. In terms of health effects on humans, the most widely studied question is whether PCBs are carcinogenic.  The EPA had a study that came out in 1996 to reassess earlier work studying this issue. On their website they state, "Studies in animals provide conclusive evidence that PCBs cause cancer. Studies in humans raise further concerns regarding the potential carcinogenicity of PCBs. Taken together, the data strongly suggest that PCBs are probable human carcinogens."

I'm so glad the US still has a regulatory agency that helps protect our environment. Well, at least at the time of this blog post, the EPA still exists. Here's the thing: PCBs are really useful. But they are also very bad for you and basically every other living organism on planet Earth. Sometimes capitalism can't have its way for the best of our bodies and our planet.

Speaking of what's best for our planet: If you care at all about Mother Earth I'll wager a guess that you already know about the massive amount of coral bleaching that's happening in the Great Barrier Reef right now. And that connection will take us to the third compound of today's aromatic medley: Tetrabromopyrrole, a coral settlement cue.

Tetrabromopyrrole, a coral settlement cue. It's got bromine atoms AND an aromatic/planar ring. Woo hoo!

Tetrabromopyrrole, a coral settlement cue. It's got bromine atoms AND an aromatic/planar ring. Woo hoo!

 

Corals are strange! Stony corals form the skeleton, literally, of the colorful corals that make some islands vacation destinations. When coral reefs are growing anew or recovering from damage, a key part of the growing process is the recruitment of coral larvae. These larvae can come from the coral that's already there (the brooders) or from the surrounding waters (broadcast spawners). In order to settle in a particular spot, the sponge larvae need a cue that it's a good location: the integration of physical and chemical cues is a complicated process that's not completely understood. After settling in the desired spot, the larvae also need to metamorphose from larvae into juvenile coral. "Complete settlement" involves both initial attachment and metamorphosis.

Researchers discovered in 2014 that a complete settlement cue for Carribean sponges (e.g. Porites astreoides) is tetrabromopyrrole. They found that this small molecule is produced by biofilm bacteria that naturally associate with coral communities, such as Pseudoalteromonas sp. PS5. Tetrabromopyrrole was a cue compound for both brooder and broadcast spawner coral larvae and has been found in other studies to induce metamorphosis in Pacific sponges. The authors speculate that given the lifelong association of proteobacteria like Pseudoalteromonas sp. PS5 with corals, and the ability of these bacteria to ward of coral pathogens through the production of other bioactive compounds, the tetrabromopyrrole cue may be a cue for the presence of a healthy and supportive bacterial biofilm community, which is essential to the survival of coral.

In conclusion: there are lots of bioactive compounds out there in the world and, like in great music, public policy, and the fine print on your iTunes agreement, the devil's in the details when it comes to chemical ecology.