|Thiaminases break thiamine in two at the red blotch I hastily added with Photoshop|
A limited yet diverse collection of organisms are capable of splitting apart vitamin B1, which also goes by thiamine (or thiamin), as a result of their ability to produce enzymes called thiaminases. Organisms feeding on thiaminase producers can end up deficient in thiamine, which is a pretty bad situation to be in. Many of the enzymes used by cells to process carbohydrates and obtain energy need to be connected with a thiamine molecule in order to work properly, so a lack of the vitamin can cause cells to off themselves via a process called apoptosis.
Animals known to occasionally become ill after consuming thiaminase-producing organisms include predatory fishes found in the Baltic Sea and the Great Lakes, American alligators, birds, and several mammals including humans. A deficiency in thiamine can result in impaired reproduction and damage to the brain and heart.
In the mid 20th century, fox and mink fur farmers ended up with sick animals after inadvertently feeding them a bunch of thiaminase-containing raw fish. This condition was called Chastek's paralysis after the farmer who reported the problem.
In the Great Lakes, lake trout (Salvelinus namaycush) are known to feed on non-native fish containing high levels of thiaminase. One such prey fish is the alewife (Alosa pseudoharengus). The resulting vitamin deficiency has been linked to deaths in both fry and adult fish, as well as various problems such as becoming really bad at capturing prey and avoiding being eaten. This is particularly annoying because we've been trying to restore lake trout populations throughout the Great Lakes.
Grazing animals (sheep, cattle, horses, goats) tend to be poisoned when they eat horsetail (genus Equisetum), bracken fern (Pteridium aquilinum), or nardoo fern (Marsilea drummondii), all which produce the vitamin-destroying enzyme. The first two are found all over the world, while the third is native to Australia.
In western Nigeria, eating the larvae of a tree-eating moth (Anaphe venata) has historically caused folks to develop cerebellar ataxia (a flu-like illness accompanied by tremors) during the rainy season (July-October) when the larvae are easy to find at local markets. The larvae, which represent a rich source of amino acids (comparable to chicken eggs), are typically roasted and added to a stew. Unfortunately, they also contain a heat-resistant thiaminase that happily continues to break apart thiamine at temperatures in excess of 70°C, making it challenging to destroy the enzyme by cooking. In better news, the illness is usually self-limiting and can be treated with thiamine.
|Vitamin-hating nardoo hanging out in a wet spot (Source)|
Another example of human thiaminase poisoning occurred among members of the Burke and Wills expedition across Australia in the later part of the 19th century. It was one of those classic European explorer tragedy deals. They ran out of food and decided to chew on the spore cases (sporocarps) of the aforementioned nardoo fern, an aquatic plant that happened to be full of thiaminase. They likely did this because they had seen the local Aboriginal peoples using the spore cases to make flour. Tragically, expedition members failed to realize the need to detoxify the plant by grinding it up into a powder and then washing it with lots of water and/or thoroughly cooking it to remove/destroy the enzyme. Several members are assumed to have died of beriberi.
The ability to produce thiaminases is sprinkled throughout the tree of life, being found in prokaryotes and eukaryotes alike. There are at least two forms of the enzyme (I and II), which appear to have arisen through convergent evolution (similar structure and function, yet made up of differing number and type of amino acids). In particular, thiaminase I is made by bacteria, protozoa, insects, shellfish (e.g. freshwater mussels), fish (e.g. carp), and ferns. Its seemingly random distribution has been suggested to be the result of the gene encoding the enzyme jumping between unrelated organisms and sticking around because it's a useful defence mechanism. The enzyme, being capable of inducing apoptosis via thiamine deficiency, may also have a role in insect metamorphosis (which involves a lot of cell turnover).
Naegleria gruberi is a single-celled protozoan hanging out in lakes, rivers, and wet soils all over the world. If there isn't much food available, the otherwise amoeba-shaped organism can sprout flagella (think sperm tails) and swim off in search of a better life. Scientists playing around with N. gruberi in labs have shown it produces a thiaminase capable of killing vertebrate cells. These include drug-resistant cancer cells, sparking interest in employing the thiaminase to wreak havoc on persistent tumours.
Some strains of Clostridium botulinum, one of the bacteria responsible for the potentially deadly condition of botulism, produce both a neurotoxin (botulinum neurotoxin A) as well as thiaminase I. The neurotoxin causes paralysis by interrupting communication between the nervous system and muscles throughout the body (by stopping the release of the neurotransmitter acetylcholine), which can lead to the inability to breathe and thus death. There are several types of botulism, one of which occurs specifically in infants. Since the community of bacteria inside a baby's intestines is still developing, it's susceptible to being taken over by C. botulinum, leading to exposure to both botulinum neurotoxin A and thiaminase. It appears that a resulting thiamine deficiency can worsen the paralysis, so giving those afflicted with botulism a high dose of thiamine could help to increase their rate of recovery. One link between botulism and thiamine deficiency is the essential role of thiamine in the synthesis of acetylcholine within nerves, the release of which is inhibited by botulinum toxin. Both the enzyme and the toxin can thus reduce the availability of acetylcholine to mediate brain-muscle communication.
Blakeslee CJ, Sweet SA, Galbraith HS, Honeyfield DC. 2015. Thiaminase activity in native freshwater mussels. Journal of Great Lakes Research 41(2):516-519.
Kraft CE, Gordon ER, Angert ER. 2014. A rapid method for assaying thiaminase I activity in diverse biological samples. PLoS One 9(3):e92688. [Full text]
Kreinbring CA, Remillard SP, Hubbard P, Brodkin HR, Leeper FJ, Hawksley D, Lai EY, Fulton C, Petsko GA, Ringe D. 2014. Structure of a eukaryotic thiaminase I. PNAS 111(1):137-142. [Full text]
Moyo AA, Bimbo FM, Adeyoyin KM, Nnaemeka AV, Oluwatoyin G, Oladeji AV. 2014. Seasonal ataxia: A case report of a disappearing disease. African Health Sciences 14(3):769-771. [Full text]
Nishimune T, Watanabe Y, Okazaki H, Akai H. 2000. Thiamin is decomposed due to Anaphe spp. entomophagy in seasonal ataxia patients in Nigeria. Journal of Nutrition 130(6):1625-1628. [Full text]
Ringe H, Schuelke M, Weber S, Dorner BG, Kirchner S, Dorner MB. 2014. Infant botulism: Is there an association with thiamine deficiency? Pediatrics 134(5):e1436-e1440.
Ross JP, Honeyfield DC, Brown SB, Brown LR, Waddle AR, Welker ME, Schoeb TR. 2009. Gizzard shad thiaminase activity and its effect on the thiamine status of captive American alligators Alligator mississippiensis. Journal of Aquatic Animal Health 21(4):239-248.