Growing Sea Lamprey Embryos Dramatically Alter Genomes, Discard Millions Of Units Of DNA

Researchers have discovered that the sea lamprey, which emerged from jawless fish first appearing 500 million years ago, dramatically remodels its genome. Shortly after a fertilized lamprey egg divides into several cells, the growing embryo discards millions of units of its DNA.

The findings were published this month in the Proceedings of the National Academy of Sciences. The lead author is Jeramiah Smith, a postdoctoral fellow in genome sciences at the University of Washington (UW) working in the Benaroya Research Institute laboratory of Chris Amemiya, who is also a UW affiliate professor of iology.
Theirs is believed to be the first recorded observation of a vertebrate -- an animal with a spinal column -- extensively reorganizing its genome as a normal part of development. A few invertebrate species, like some roundworms, have been shown to undergo extensive genome remodeling. However, stability was thought to be vital in vertebrates' genomes to assure their highly precise, normal functioning. Only slight modifications to allow for immune response were believed to occur in the vertebrate genome, not broad-scale rearrangements.
Smith, Amemiya and their research team inadvertently discovered the dynamic transformations in the sea lamprey genome while studying the genetic origins of its immune system. The researchers were trying to deduce how the sea lamprey employs a copy-and-paste mechanism to generate diverse receptors for detecting a variety of pathogens.
The researchers were surprised to notice a difference between the genome structure in the germline -- the cells that become eggs and the sperm that fertilize them -- and the genome structure in the resulting embryonic cells. The DNA in the early embryonic cells had myriad breaks that resembled those in dying cells …but the cells weren't dying. The embryonic cells had considerably fewer repeat DNA sequences than did the sperm cells and their precursors.
"The remodeling begins at the point when the embryo turns on its own genes and no longer relies on its mom's store of mRNA," said Smith.
The restructuring doesn't occur all at once, but continues for a long while during embryonic development. It took at lot of work for the scientists to see what was lost and when. They learned, among other findings, that the remodeled genome had fewer repeats and specific gene-encoding sequences. Deletions along the strands of DNA are also thought to move certain regulatory switches in the genome closer to previously distant segments.
The scientists don't know how this happens, or why. Smith said that his favorite hypothesis, yet unproven, is that the extra genetic material might play a role in the proliferation of precursor cells for sperm and eggs, and in early embryonic development. The genetic material might then be discarded either when it is no longer needed or to prevent abnormal growth.
The alteration of the sea lamprey genome and of invertebrates that restructure their genome appears to be tightly regulated, according to Smith, yet the resulting structural changes seem almost like the DNA errors that give rise to cancers or other genomic disorders in higher animals. Learning how sea lamprey DNA rearrangements are regulated during development might provide information on what stabilizes or changes the genome, he said, as well the role of restructuring in helping form different types of body cells, like fin, muscle, or liver cells.
If 20 percent of their genome disappears, how do sea lampreys pass along the full complement of their genes to their offspring?
"The germline -- those precursor cells for sperm and eggs -- is a continuous lineage through time," Smith explained. "The precursor cells for sperm and egg are set apart early in lamprey development. The genome in that cell population should never change." Genetic material is assumed to be lost only in the early embryonic cells destined to become body parts and not in cells that give rise to the next generation. The researchers have been looking for the primordial stem cells for sperm and eggs hidden away in the lamprey, but they are difficult to find.
Researchers do not yet know how the sea lamprey's genome guides the morphing it undergoes during its life. Sea lampreys have a long juvenile life as larvae in fresh water, where they eat on their own. Their short adult lives are normally spent in the sea as blood-sucking parasites. Their round, jawless mouths stick like suction cups to other fish. Several circular rows of teeth rasp through the skin of their unlucky hosts. Their appetite is voracious.
Later, as they return to streams and rivers along the northern Atlantic seaboard, sea lampreys atrophy until they are little more than vehicles for reproduction. After mating, they perish. Populations of sea lamprey were landlocked in the Great Lakes and other nearby large lakes after canals and dams were built in the early 1900's. They thrive by parasitizing (and killing) commercially important fish species and are considered a nuisance in the Great Lakes region.
Biologists are interested in the sea lamprey partly because of its alternating lifestyles, but largely because it represents a living fossil from around the time vertebrates originated. Close relatives of sea lampreys were on earth before the dinosaurs. It's possible that the sea lamprey's dynamic genome biology might someday be traced back in evolutionary history to a point near, and perhaps including, a common ancestor of all vertebrates living today, the authors of the study noted.
"Sea lampreys have a half billion years of evolutionary history," Smith said. "Evolutionary biologists and geneticists can compare their genomes to other vertebrates and humans to see what parts of the lamprey genome might have been present in our primitive ancestors. We might begin to understand how changes in the sea lamprey genome led to their distinct body structure and how fishes evolved from jawless to jawed."
Amemiya added, "We don't really know where this discovery about the sea lamprey's remodeling of its genome will take us. It's common in science for the implications of a finding not to be realized for several decades. It's less about connecting the dots to a specific application, and more about obtaining a broad understanding of how living things are put together."
In addition to Smith and Amemiya, the other researchers on this study were Francesca Antonacci and Evan E. Eichler of the UW Department of Genome Sciences. Research grants from the National Institutes of Health,the National Science Foundation and the Howard Hughes Medical Institute funded the project. Smith also received National Research Service Awards, including an Institutional Ruth L. Krischstein Award through the University of Washington Department of Genome Sciences and an individual Ruth L. Krischstein Award through the National Institute of General Medical Sciences.
Adapted from materials provided by University of Washington.

Rare fish 'proves water quality'

Lampreys are extremely selective with their spawning sites The discovery of a rare blood-sucking fish in the River Wear is proof of high water quality, conservationists said.Seven adult sea lampreys, which have toothed, funnel-like sucking mouths, have been found in the river near Chester-le-Street, County Durham. Only three species of lampreys remain in Britain, and they are protected under European law. The Environment Agency said the creatures only breed in water which is very clean. So far the agency has identified twelve spawning sites, known as redds. Fisheries officer Paul Frear said: "We were thrilled to discover lampreys back in the River Wear, as these rare blood-suckers show us that the water quality in the river is very high. "Lampreys are extremely selective with their spawning sites and will only nest where the water quality is optimal." Scientists are continuing to search for more lampreys, and anyone who spots one is asked to report the sighting to the Environment Agency.BBC News

Evolution Of A Contraceptive For Invasive Sea Lamprey

In addition to providing fundamental insights into the early evolution of the estrogen receptor, research by a team at the University of California, San Diego School of Medicine may lead to a contraceptive for female lampreys – a jawless fish considered an invasive pest species in the Great Lakes region of the United States. This could prove important to the Great Lakes region, where lampreys aggressively consume trout, salmon, sturgeon and other game fish.

"Since the introduction of sea lamprey to the Great Lakes, the fisheries have been devastated, and as a result, there is much interest in finding new methods to control the lamprey population," said Michael E. Baker, PhD, professor in UC San Diego's Department of Medicine, Division of Nephrology-Hypertension. "Our research could lead to a contraceptive for female lamprey, providing a method to control their reproduction in the Great Lakes." The researchers' findings will be published by PloS ONE on June 25.
Lampreys evolved about 450 million years ago, before the appearance of sharks. In contrast to sharks, fish and land vertebrates, lampreys have no jaw. They feed on fish by attaching themselves to the fish and sucking their body fluids. Their aggressive consumption of game fish has eliminated many natural predators of the alewife, another invasive species on the Great Lakes. This has allowed the alewife population to explode, with adverse effects on many native fish species.
As part of a program to understand the evolution of steroid hormone signaling, the UC San Diego researchers characterized the estrogen-binding site on the estrogen receptor in the sea lamprey. To accomplish this, Baker – along with David Chang, student in the UC San Diego Department of Biology, and Charlie Chandsawangbhuwana, graduate student of Bioengineering in UC San Diego's Jacobs School of Engineering – constructed a 3-D model of the structure of the lamprey estrogen receptor.
The active estrogen in lamprey is unknown, although recent research in the field suggested that lamprey estrogens contain a 15alpha-hydroxyl group, which is lacking in other types of vertebrate estrogen. The model developed by the UC San Diego research team uncovered a unique interaction between 15alpha-hydroxy-estradiol and an amino acid called methionine, found only in lamprey estrogen receptors.
"The unique aspect of this interaction suggests that there are compounds that can bind specifically to the lamprey estrogen receptor, but not to estrogen receptors in other animals," said Baker, adding that some of these compounds could interfere with estrogen action and act as contraceptives in female lamprey, providing a method to control their numbers.
Adapted from materials provided by University of California - San Diego, via EurekAlert!, a service of AAAS.

MSU scientists hope love potion lures lampreys

East Lansing, MI ... The patented pheromone has been more than a decade in the making. It's a copy of a scent male sea lampreys, a highly destructive invasive species, send out into streams during mating season to draw females to their nests.Although scientists have copied and used pheromones in the insect world for pest control, no one has ever tried it on fish or any other vertebrates before, said research ecologist Nick Johnson of the Hammond Bay Biological Station in the Upper Peninsula.Starting nearly two weeks ago and continuing most nights through June, Johnson and helpers are testing the love scent by pumping small doses of the pheromone through existing traps into specific rivers in northern Michigan.Lampreys are born in these streams and return to mate. Johnson's earlier research, while he was a student at Michigan State University, where the pheromone was developed, showed that females will swim upstream long distances hunting for the pheromone's source, straight into traps."Once they smell it, they follow it," Johnson said.Researchers check the traps every day or two to see how many lampreys they have lured. After warm spring nights, when mating lampreys are most active, Johnson expects to find as many as 500 lampreys in a trap. Once trapped, the females are destroyed or used in research. They won't produce any offspring, and that's key."To control the population, we want to remove the females," Johnson said.Unchanged creatureSea lampreys, a species that has survived nearly unchanged for 400 million to 500 million years, are native to the Atlantic Ocean. Scientists believe the lampreys migrated into the Great Lakes after locks and canals bypassing Niagara Falls were built. Since they have no predators in the Great Lakes, once established, they flourished.The lampreys prey on soft-fleshed native fish like lake trout and whitefish, attaching sucker mouths to their sides and feeding on their bodily fluids. The fish usually die.(2 of 2)After lampreys showed up in Lake Huron in the 1920s, they spread throughout the upper Great Lakes, devastating various fish species, including lake trout, by the 1950s. Since those fish were predators of invasive alewives, their loss led to an explosion of alewives.Since 1958, the main weapon against lampreys has been a chemical compound known as TFM, which kills the slippery fish when they're still young larvae in streams. It is safe for other species but expensive. The Great Lakes Fishery Commission, created in 1955 mainly to control sea lampreys, spends most of its $18-million budget on the lampricide program, said Mike Siefkes, sea lamprey specialist for the commission.Lampricide is hard to use on large rivers like the St. Mary's River in the Upper Peninsula, which leads into Lake Huron. The Hammond Bay Biological Station traps male lampreys in that river, sterilizes them with a chemical compound and releases them to mate with fertile females. Males and females die after they mate, so the lamprey couple will not reproduce.Barriers usedTFM, barriers that halt their movement and sterilization have brought lamprey numbers down to 10 percent of their peak of five million decades ago, Siefkes said. "But we need to keep on it, or they'll bounce back," he said. There still are too many lampreys in lakes Michigan and Huron, although the population is better controlled in Lake Superior and native fish are returning there, he said.Into smaller riversIf the love potion works, the traps could catch large numbers of lampreys.The pheromone also might be used to lure spawning lampreys out of rivers too large to treat with lampricide and into smaller rivers where the chemical can work, said Johnson."There are lots of strategies we could use," Johnson said.The pheromone is so potent that only miniscule amounts are needed, so it could be a cheaper alternative to lampricides, Johnson said.For now, all the research on pheromones is being done in Michigan. Besides 3-kPZS, MSU has ongoing research on other pheromones, including one that young lampreys emit into streams as larvae. That pheromone tells adults which streams to return to later to spawn.If the pheromones work in the wild, it could be a groundbreaking step, not just for lamprey control but other invasive species, Siefkes said.

Sex smell lures 'vampire' to doom

The sea lamprey's mouth has garnered it the nickname "vampire fish" A synthetic "chemical sex smell" could help rid North America's Great Lakes of a devastating pest, scientists say. US researchers deployed a laboratory version of a male sea lamprey pheromone to trick ovulating females into swimming upstream into traps. The sea lamprey, sometimes dubbed the "vampire fish", has parasitised native species of the Great Lakes since its accidental introduction in the 1800s. The work is reported in Proceedings of the National Academy of Sciences. The Great Lakes on the US-Canada border support recreational fishing worth billions of dollars a year, which the lampreys would wreck but for a control programme costing about $20m annually. This is thought to be the first time that pheromones have been shown to be the basis of a possible way of controlling animal pests other than insects. "There's been extensive study of pheromones in animals and even in humans," said lead researcher Weiming Li from Michigan State University in East Lansing, US. It was one of the worst things to hit the Great Lakes in the history of European settlement Marc Gaden "But most researchers have presumed that as animals get more complex, their behaviour is regulated in a more complex way, not by just one pheromone," he told BBC News. Professor Li's team released the synthetic version of a lamprey hormone from a trap placed in a stream where lampreys come to breed. Females scenting it would swim vigorously upstream until they found the source, some becoming trapped in the process. Death wish The sea lamprey's natural life cycle takes it from birth in a stream to adulthood in the ocean, where it gains its vampirical appellation. Circular jaws lock on to another, larger fish, and a sharp tongue carves through its scales. >From then on the lamprey feeds on the blood and body fluids of its temporary host, often killing it in the process. Eventually, the satiated lampreys - both males and females - find a suitable stream to swim up, breed and die. The female lampreys were lured into traps on the stream Unlike salmon, which seek out the stream they were born in, lampreys appear willing to take any stream indicating a suitable breeding place; and perhaps pheromones play a role in identifying streams worth selecting. In their native Atlantic Ocean, their numbers are controlled by predation; but in the Great Lakes they have no predators. They first appeared in the 1800s after completion of the Erie Canal linking the lakes to New York. Colonisation was completed a century later when other canals provided unfettered access to the upper lakes. What followed was decimation of native fish. "It was one of the worst things to hit the Great Lakes in the history of European settlement," said Marc Gaden from the Great Lakes Fishery Commission (GLFC), the body responsible for controlling the lamprey problem. "Before it, we had a thriving fishery largely dependent on native fish such as the lake trout... but by 1940 they had colonised thousands of streams and fishermen were beginning to see the devastation." Getting fresh Many fish can survive only in fresh water or only in the oceans - or, like salmon, have a set migration between the two - but the lamprey appears to have thrived on its move from the saline Atlantic to the fresh environs of the five lakes. Each individual devours a total weight of up to 20kg of trout or other host fish during its parasitic lifetime. The GLFC has established a complex set of control measures, including dusting the streams with pesticides specific to the lamprey, building barriers to block their upstream migration, and releasing sterile males to reduce breeding. "Why we're so enthusiastic about the pheromone work is that we see it as another tool in the arsenal," said Dr Gaden. "We see it as away of tricking these spawning lampreys, and then you can do things to manipulate their behaviour in ways that would work against them - for example you could lure them into streams without suitable spawning habitat, or just into traps." Professor Li's team is now planning a larger experiment, using the pheromone to trap female lampreys in 20 streams feeding into the lakes, which will take three years to complete.