Sea lampreys are masters of transformation. These ancient fish begin life as tiny worm-like creatures that bury in sandy riverbeds and filter food particles out of the water. However, after years of sedentary existence, lampreys undergo a dramatic metamorphosis; just like caterpillars turn into butterflies, lamprey larvae turn into, well, something less gorgeous. The fish grow larger, become active eel-like swimmers and leave their sandy homes to migrate out to sea. Once in the ocean, filter-feeding is passé and lampreys transform their mouths into a suction cup with alien-looking, circular rows of teeth that latch on to larger fish, pierce their skin and suck their blood; a rare case of parasitism in a vertebrate. However, these lifestyle changes come at a price. The saltier water in the ocean requires a complete overhaul of the gills, which handle the internal salt balance of fish. And, the digestion of a blood meal, which is extremely rich in protein, produces toxic ammonia that needs to be cleared into the water, through the gills. Julia Sunga and her colleagues at Wilfrid Laurier University, Canada, set about investigating how lampreys remodel their gills during metamorphosis to accommodate their new parasitic lifestyle.

In the lab, the team either held maturing lampreys in freshwater or transferred them to seawater to simulate their natural ocean migration. In addition, to study the change in diet, the team kept one group of lampreys in a tank together with some hapless rainbow trout that would serve as prey. The researchers then measured how much toxic ammonia had built up in the lampreys’ blood and how much they released into the water.

Over the course of the lampreys’ development, the quantity of toxic ammonia in their blood increased and was highest after metamorphosis. However, the amount of ammonia released into the water changed little throughout metamorphosis and was unaffected by whether the animals were held in freshwater or seawater. Even more surprisingly, those parasitic lampreys that were feasting on the blood of trout released 5 times more ammonia into the water than the lampreys that were not dining and this kept the levels of ammonia in their blood very low. To find out how, the researchers zoomed in on their gills.

Immunohistochemistry revealed that larval lamprey gills were covered in rhesus glycoproteins, small channels that can funnel ammonia across cell membranes. The researchers also found a proton pump that generates acidic conditions around the channels to promote the removal of ammonia from the lampreys’ blood, expelling it into freshwater. However, during metamorphosis, these proteins began to disappear. Instead, new cells started to develop, packed with power-generating mitochondria, which would maintain the lampreys’ salt balance in seawater. These new cells had their own ammonia channels, only this time, they were linked to a sodium/potassium pump. Under the microscope, the two proteins seemed to overlap perfectly within the cells, especially in lamprey that had been feasting on blood. Thus, it seems that lamprey have a broad toolkit at their disposal to clear ammonia from their blood, which they adjust throughout development, based on the salinity of the water and their preferred diet.

Lampreys are ancient creatures that pre-date the evolution of jaws and their intricate life cycle spans a broad range of habitats, appearances, behaviours and diets. This close look at the gills of developing lampreys revealed the surprisingly flexible machinery that allows the versatile creatures to maintain salt balance and ammonia excretion throughout their changing lifestyle. A lamprey's transformation may be less pretty than that of a butterfly but, nonetheless, parasitic lamprey are awe-inspiring creatures, just in a nightmarish kind of way.

References

References
Sunga
,
J.
,
Wilson
,
J. M.
and
Wilkie
,
M. P.
(
2020
).
Functional re-organization of the gills of metamorphosing sea lamprey (Petromyzon marinus): preparation for a blood diet and the freshwater to seawater transition
.
J. Comp. Physiol. B.
.