How does a fungus know which way is up? For one group of fungi, it’s the same way that people do: build some big crystals, let them sink under gravity, then sense which part of their container they settle upon. Now you know which way is Earth, and which way is Sky.
What is extraordinary about this is that members of three mighty kingdoms – Plants, Animals, and Fungi – all appear to have stumbled on the same solution independently. And, in the case of mucoralean fungi, they appear to have constructed their system from parts lifted from yet another kingdom – Bacteria – where they weren't being used for that purpose at all.
The purloined protein in question, OCTIN – octahedral crystal matrix protein – forms short chains within bacteria. It does this in the periplasm, a gel-filled space between their inner and outer cell membranes (a thin cell wall is also located here in Gram-negative bacteria). What bacteria do -- if anything -- with OCTIN remains mysterious.
But based on the calculated size, weight and density of bacterial OCTIN; the density and viscosity of the periplasmic fluid in which it’s found; and the cramped space in which it exists, it seems highly unlikely bacteria are using it to sense gravity, the authors of a new study write in the journal PLoS Biology. Brownian motion -- the random movement of molecules in a fluid -- dominates the effects of gravity at this scale, they found. And even if it didn’t, there simply isn’t room in the periplasm for OCTIN to go anywhere in response to gravity. Finally, why would most bacteria even care about sensing it?
Plants and fungi, on the other hand, make big, expensive structures – shoots, leaves, mushrooms, and sporangia -- that only work correctly when properly oriented with respect to Earth's core. Plants and fungi use their gravity sensors to send “grow this way” signals to the cells in these structures to ensure correct placement (I wrote about plant gravity sensing previously here).
Plants use big starch grains for the purpose, while humans and other vertebrates (which have very different reasons for caring about which way is up) use calcium carbonate crystals called otoliths. No one yet knows exactly how the mushroom fungi do it, but another group of fungi called the Mucorales – which includes the common bread mold Rhizopus stolonifer — sense gravity in their giant single-celled spore-making stalks.
The member of the group that has been well-studied – Phycomyces blakesleeanus -- uses a combination of massive octahedral OCTIN crystals and buoyant fat globs inside a bag called a vacuole to tell which way is up. But there’s something fishy about that OCTIN.
The scientists compared the DNA sequence of fungal OCTIN to bacterial OCTIN and decided it’s likely they share a common origin, and that origin was the gram-negative bacteria. Because similar gravity-sensing structures have been seen in other Mucoralean fungi, it’s likely the entire fungal group acquired OCTIN from bacteria early in their evolution. Yes, that's not "supposed" to happen. We'll get back to that in a minute.
Because there's another aspect of fungal OCTIN that's a real head-scratcher if its origin was indeed bacterial. OCTIN crystals inside Phycomyces are so huge – around 5 micrometers wide -- that they are larger than many entire bacteria. The bacteria from which OCTIN was likely stolen range from 0.3 to 0.8 micrometers in diameter. So the fungal incarnation of this protein polymer is roughly 10 times as large as the bacteria from which it came. Something pretty crazy happened to OCTIN inside mucoralean fungi.
Both bacterial and fungal OCTIN link into chains using disulfide bonds, which suggests fungi did retain the assembly mechanism employed by bacteria. The ability to form these short chains probably made it a good candidate for a future gravity sensor as making long chains instead of short chains probably wasn’t a difficult leap. But fungi took things further by somehow catalyzing the crafting of titanic protein crystals, creating the sensory apparatus to detect the response of those crystals to gravity, and addressing OCTIN proteins or the fully-assembled OCTIN crystals so that they get delivered to that sensor from their manufacturing site. It's a nifty piece of work.
So just how did that OCTIN end up in fungi in the first place? A certain amount of gene swapping, biologists have come to understand, is par for the course on Earth, even between organisms very distantly related. This phenomenon is referred to as horizontal gene transfer, and, like the discovery of microbiota and of epigenetics, it has thrown traditional Mendelian genetics and inheritance for a loop. It’s not that the majority of our genes aren’t inherited from our parents and that those genes aren’t foremost in determining what we are. It’s just that there turn out to be a rather large number of asterisks. Inter-domain gene stealing is a big one.
How does it work? In bacteria, foreign genes may arrive inside new hosts by random uptake of naked DNA floating in the environment (bacteria have a relatively cavalier attitude toward the sanctity of their DNA); through marauding viruses that have picked them up in previous hosts and deposit them in a new host’s genome; or via bacterial sex, also called conjugation.
Eukaryotes – all large life on Earth and also many small ones containing nuclei – may also use the first two methods. Or perhaps when they eat, some of their prey's DNA may escape digestion and go on to find salvation through insertion in the predator’s genome. There may be other ways too.
Why would early Mucoralean fungi have held on to what was at first an apparently useless new protein? It’s possible that the cost to maintain it was very small and so there was no strong selection against it, an idea called neutral selection. Or perhaps it performed some sort of other valuable enzymatic activity – enzymes facilitate important chemical reactions -- in both bacteria and fungi that’s not yet obvious.
Still, this particular instance of horizontal gene transfer is surprising. Usually, horizontal gene transfer is a straightforward process in which one organism steals a useful gene from another and then uses it for pretty much the same purpose. Frequent targets of opportunity include antibiotic resistance genes, virulence-promoting factors, useful enzymes, and proteins that help their owners endure environmental extremes. This example seems to show that something else is possible: stolen genes can be used to construct something truly innovative. If so, it would be no different from how evolution operates on genes acquired by the usual method: from parents.
Nguyen TA, Greig J, Khan A, Goh C, Jedd G (2018) Evolutionary novelty in gravity sensing through horizontal gene transfer and high-order protein assembly. PLoS Biol 16(4): e2004920.