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Hot Topic Origins Extreme Life Tandem Evolution
Tandem Evolution
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Extreme Life
Posted:   06/03/02
Author:    Anne M. Rosenthal

Summary: A type of clam that inhabits deep-sea hydrothermal vents is so closely knit with a bacterium living in its tissues that their evolutionary paths, as recorded in their DNA, run in lockstep.


Vesicomyid Clam
Vesicomyid clams are are just some of the fauna found near hydrothermal vents that depend on chemosynthesis to obtain energy.
Credit: Department of Marine Environmental Geology
Several kilometers beneath the ocean surface a fascinating evolutionary synchrony is occurring. A type of clam that inhabits deep-sea hydrothermal vents is so closely knit with a bacterium living in its tissues that their evolutionary paths, as recorded in their DNA, run in lockstep.

Vesicomyid clams are some of the many intriguing animals inhabiting hydrothermal vents. Like other vent fauna, they depend on sulfide-eating microbes for energy. Sunlight does not penetrate to the ocean's depths. In its absence, photosynthesis the powerhouse for food chains on the Earth's surface cannot occur.

Instead, the sulfur bacteria obtain energy through a process called chemosynthesis. They oxidize hydrogen sulfide (H2S) from mineral-rich underwater flows, using the energy released by this chemical reaction to build organic compounds. Because higher organisms can use these organic compounds for food, the sulfur bacteria form the base of the food chain for vent fauna.

Many hydrothermal vent animals graze on free-living forms of these sulfur bacteria, which grow in such profusion that the colonies appear almost like grass growing around the vents. But vesicomyid clams, like the giant tubeworms and mussels that also inhabit the vents, host sulfur bacteria within their own tissues. In a symbiotic relationship, the bacteria provide their hosts with nutrients while their hosts provide a specialized environment where the bacteria can flourish.

A Maternal Inheritance

This symbiosis has intrigued several researchers, including Dr. Robert Vrijenhoek, a biologist at the Monterey Bay Aquarium Research Institute (MBARI), who studies genetic variation among hydrothermal vent organisms. "Symbiosis is interesting because it contrasts with pathogenesis," Vrijenhoek says. "Studying negative and positive interactions between bacteria and hosts can provide insights regarding the evolutionary dynamics of bacteria."

Vrijenhoek began looking more closely at the clams and their bacterial guests. In earlier studies, species of sulfur bacteria residing within vesicomyid clams were found only as symbionts, never as free-living organisms. Studies by S. Craig Cary, Professor at the University of Delaware, College of Marine Studies, suggested that rather than obtaining bacteria from the surrounding water, the clams inherited their microbes from their mothers: The eggs from which the clams developed contained bacterial starter cultures.

The obligatory symbiosis between the clams and their bacteria neither can survive without the other predisposes them to a tight evolutionary relationship. Vrijenhoek's group, which was then at Rutgers University and included Andrew Peek, Robert Feldman, and Richard Lutz, hypothesized that the two evolved together, a process known as coevolution. "Symbiosis is one of the most important issues in coevolution," notes Vrijenhoek, "with both the hosts and symbionts evolving to improve the way they cooperate."

Vesicomyid clam
The bacteria that exists inside the clams may have evolved togehter with the clams. If the clam and bacterial species had coevolved, their evolutionary trees could have the same basic shapes.
Credit: Department of Marine Environmental Geology



Over the eons, when one species of clam evolved into two perhaps through the isolation of one population from another, or the colonization of greater depths the bacterial strain riding along would also have split into two lineages that scientists might identify as distinct species. The branching of one or more species from another forms what can be pictured as an evolutionary tree.

"The ancestors form the roots, the trunk, and the branches, successively, and modern, that is, living species form the twigs at the ends of this tree. Some branches are broken - species go extinct, terminating a branch - and others proliferate wildly into many twigs since speciation can occur in rapid bursts," Vrijenhoek explains.

Vrijenhoek's group proposed that if the clam and bacterial species had coevolved, their evolutionary trees should have the same basic shapes. They used molecular biology techniques to examine the DNA and construct genealogies evolutionary trees of genes for both the clams and their guests.

"The mechanism by which the clams obtain their bacteria, maternal inheritance, is significant," says Vrijenhoek, "because it would tend to preserve any genetic signature of coevolution by the two species. No contamination of the clams with new bacteria from the environment would dilute the signature."

Matching Trees

The first step was to obtain a variety of clam species. Vrijenhoek's group was able to obtain specimens of nine different species from hydrothermal vent communities distributed worldwide.

To construct the evolutionary tree for the bacteria, the scientists looked for variations in portions of the bacterial chromosome that code for ribosomes, the cellular structures where amino acid chains are manufactured.

For the clams, the scientists chose segments from mitochondrial DNA. Mitochondria are small organelles that exist within the cells of all multicellular organisms. These organelles have their own DNA and are inherited maternally through the egg, similar to the way in which the symbiotic bacteria are inherited from one hydrothermal clam generation to another. Therefore, if coevolution had occurred, changes in bacterial DNA, as mapped in an evolutionary tree, would likely be mirrored in clam mitochondrial DNA.

The findings were spectacular. The trees for the clams and their sulfur bacteria matched closely, both in their branching patterns and the evolutionary times when new species developed. Cospeciation- new species arising together- had, indeed, occurred.

A Different Strategy

Vrijenhoek's group also wondered about other vent animals with bacterial symbionts. Had coevolution occurred there as well? The group decided to focus next on vestimentiferan tubeworms.

In previous studies led by Cary, examination of tubeworm eggs had yielded no bacteria. The scientists worried, however, that perhaps sulfur bacteria were present in those eggs, just difficult to detect with the available techniques. Thus, Cary joined his efforts with Vrijenhoek's group to determine whether the tubeworms obtained their bacteria from surrounding waters.

The sulfur bacteria hosted by tubeworms are different than those found in vesicomyid clams. Robert Feldman, then a Rutgers University postdoctoral fellow working with Vrijenhoek and Cary, found that the species of bacterium a tubeworm hosts depends on the worm's habitat. Species of tubeworms that lived on basaltic vents all shared one type of bacterium, while species of tubeworms that lived in muddy sediments all shared another.

tubeworms
Tubeworms have no mouth, eyes, or stomach ("gut"). Their survival depends on a symbiotic relationship with the billions of bacteria that live inside of them.
Credit: University of Delaware Graduate College of Marine Studies



Using genetic techniques capable of finer levels of discrimination, Carol DiMeo, then a graduate student at the University of Delaware, found that all the tubeworm species living near a particular vent hosted the same set of bacterial strains. "These findings lent further support to the supposition that tubeworms are reinfected in every generation from the surrounding environment," explains Vrijenhoek.

Without a means of inheriting their bacteria, the evolution of tubeworm species likely occurred independently of their symbionts. As in the previous study of clams, the group looked at ribosomal DNA for the bacteria, and mitochondrial DNA for their hosts. But unlike the clams and their symbionts, there was no evidence that the mitochondrial DNA of the tubeworms and ribosomal DNA of the bacteria had evolved in tandem. Not only did the evolutionary trees of the tubeworms and their bacteria differ in their branching patterns, but also speciation had occurred over vastly different time spans.

"Several groups of bivalves hosting chemosynthetic symbiotic bacteria have been studied for possible evidence of cospeciation, but Vrijenhoek's work on the vesicomyids marks the first time that cospeciation has actually been demonstrated," says Colleen Cavanaugh, Professor of Biology at Harvard University and an authority on symbiotic relationships in hydrothermal vent fauna. It was Cavanaugh who confirmed, in 1983, the presence of the symbiotic bacteria in the gill tissue of the vesicomyid clams.

"The other major groups between which symbioses have been extensively studied are insects and bacteria, especially aphids and the Buchnera bacterium," explains Cavanaugh. "Importantly, the genome of the Buchnera symbiont has been sequenced completely, allowing comparisons at many levels," between bacteria that are free-living and those that can only survive as symbionts. "Sequencing the genomes of symbionts like those hosted by vesicomyid clams," Cavanaugh adds, "could provide enormous insights into...these bacteria."

"Vesicomyid clams and vestimentiferan tubeworms exemplify two contrasting evolutionary strategies for obtaining the bacteria that allow them to survive in the hydrogen sulfide-based vent ecosystem," muses Vrijenhoek. "Each strategy confers different benefits and risks to both the host species and the bacterial species residing within them."

"Carrying the symbiotic bacterium in its eggs and larvae provides a benefit for clams that need to find far-flung hydrothermal vent habitats in a vast ocean. Dispersing clam larvae arrive at a new vent habitat with everything that's needed to grow and survive," says Vrijenhoek.

"In contrast, when tubeworm larvae disperse, not only do they have to find hydrothermal vents tiny and ephemeral habitats they also need to incorporate an appropriate species of sulfur-oxidizing bacterium before they can grow," he notes.

"Since tubeworms colonize hydrothermal vents in the eastern Pacific more rapidly and effectively than clams, acquiring a symbiont from the environment seems to pay off," Vrijenhoek says. "The clams, on the other hand, appear to wait until conditions are just right for establishment and growth of a new colony. Although the riskier strategy may pay higher rewards for the tubeworms, the safer strategy works for the clams. Both the clams and tubeworms have been participating in their respective symbiotic life style for perhaps as much as 100 million years."

What's Next

Vrijenhoek's group, including MBARI post-doctoral fellow Steven Hallam, is continuing to look at various aspects of the evolutionary relationship between deep-sea tubeworms and their symbiotic bacteria. Studies submitted for publication examine whether the ratios of bacterial strains within tubeworms are consistent across tubeworm species at a single location. These studies could provide additional insight on environmental acquisition of bacteria.

Part of Cavanaugh's current research may aid in learning about the tubeworm bacteria. She is currently funded by NOAA (National Oceanic and Atmospheric Administration) to search for free-living forms of tubeworm symbionts using the Alvin submersible, a search comparable to looking for a potential 'needle in a haystack'. So far, even though all evidence points to environmental transmission of these symbiotic bacteria, no one has isolated them from the environment.

Vrijenhoek's interests include how the tubeworm host and its symbiotic bacteria find each other, which, he says, is completely unknown. "We are hoping that the new discoveries being made with pathogenic bacteria of humans and nitrogen-fixing bacteria that infect legumes can help us develop models for environmentally acquired symbionts," says Vrijenhoek. "How do the hosts find the bacteria? Or is it the other way around?"

Vrijenhoek also wants to look at how the bacteria invade host tissues, including how the host recognizes the invaders as beneficial rather than harmful.


Related Stories

Hydrothermal Vent Life
Images from the Alvin submersible
The symbiotic relationship between vent-dwelling animals and bacteria

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