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Dissing a loaded label for some unicellular life

Prominent biologist calls ‘prokaryote’ outdated term

1:53pm, March 27, 2009
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Norman Pace has a problem with prokaryotes.

It’s not that Pace has anything against the organisms themselves. The microbiologist and RNA scientist from the University of Colorado at Boulder has made a career of studying microorganisms. It’s the term prokaryote that he doesn’t like. At the American Association for the Advancement of Science meeting in February, he said he wants to see the word abolished.

Prokaryotes are unicellular organisms, including bacteria and archaea, that don’t encase their DNA in a nucleus and do not contain membrane-bound organelles. The very name prokaryote implies that the microbes are precursors to eukaryotes —organisms that do wrap their genetic material in a nucleus and do have the organelles.

But not being something or not having certain features is not a scientific definition for what an organism is, Pace says. And the part about prokaryotes giving rise to eukaryotes? It’s wrong, he says.

“When you read in your textbooks that eukaryotes came to be 2.7 billion years ago, it is bogus,” he said at the meeting. “The eukaryote is as old as life.”

Pace’s contentious assertions are based on a tree of life compiled from comparisons of ribosomal RNA, one component of the protein-building machinery in cells. In 1977, Carl Woese of the University of Illinois at Urbana-Champaign first described three domains of life — eukaryotes, bacteria and archaea —using differences in the rRNA to determine relationships between the organisms. Woese’s genetic reclassification of life suggested not only that bacteria and archaea are distinct groups, but also that eukaryotes and archaea are more closely related than bacteria and archaea. That view is now widely accepted.

For Pace, it’s not just semantics. He says it is time to put aside the outdated concept of prokaryote and use the terms that reflect the branches of the three-domain tree. “Continued use of the term prokaryote perpetuates incorrect concepts about phylogenetic organization and evolution, the very foundations of biological thought,” Pace wrote in January 2008 in Microbe magazine.

But other biologists say Pace is in the minority and is himself working with old assumptions. Newer ways of comparing DNA, they say, show different relationships among the three domains, some of which support the idea that prokaryotes did give rise to eukaryotes.

For practical purposes prokaryote is still useful, says William “Barny” Whitman, a microbiologist at the University of Georgia in Athens. He and Pace debate the usefulness of the term in a dialog published in the April Journal of Bacteriology.

“A lot of times experimentally you can’t distinguish the archaea from bacteria,” Whitman says. “So operationally, it would be cumbersome not to have a term like prokaryote.”

He is not the only prokaryote fan.

“The ‘pro’ part of it is correct,” says Michael Dolan of the University of Massachusetts Amherst. Fossil evidence points to prokaryotes preceding eukaryotes in time, he says.

Whitman agrees. “There is no evidence that the eukaryotes are primordial,” he says. “Most of our evidence suggests that eukaryotes are fairly modern organisms and were preceded by prokaryotes.”

But Pace says fossil evidence of nuclear membranes is irrelevant in light of the genetic data. The genetic signature of eukaryotes could have existed long before the morphological trait of having a membrane around DNA, he says.

“Biology bit into a bad apple,” Pace says. “The whole issue of prokaryote-eukaryote was taken as a truth when it was still just conjecture. Prokaryote was a figment of imagination that got canonized in the institution of biology rather than the question remaining open — what are those little things? That’s an interesting question. You don’t just blow it off as prokaryote.”

Lumping bacteria and archaea into one group gives both short shrift and denies genetic and other fundamental differences between them, Pace says. For instance, archaea have a unique membrane chemistry and their cell walls are made from materials different from what either bacteria or plants use. And archaea use proteins similar to those found in eukaryotes to package their DNA, copy instructions from DNA into RNA and build proteins.

But prokaryote supporters say Pace is doing a disservice to eukaryotes.
“I think professor Pace just ignores the whole issue of the fusion of genomes that is at the heart of the evolution of eukaryotes,” Dolan says.

Genomic analyses show that eukaryotes carry structural genes — needed for building a cell and its components — from bacteria, while genes involved in informational processes, such as DNA synthesis, transcription and translation, are shared with archaea, says James Lake, an evolutionary phylogenomicist at the University of California, Los Angeles. His analysis suggests that eukaryotes are the product of a fusion of a bacterium and an archaeon.

“The basis for making a change to remove prokaryote from our vocabulary should be based on new information and analysis,” Lake says.

And newer studies that compare sets of genes other than rRNA suggest different arrangements for the tree of life. In a study in the Dec. 23 Proceedings of the National Academy of Sciences, researchers in England built many different trees of life using several statistical methods. Most of the trees don’t look like the three-domain tree Pace favors. Instead, more trees suggest that eukaryotes arose from a branch of the archaea, called the eocytes or Crenarchaeota. Bacteria occupy their own branch.
“Any discussion of the tabling of prokaryotes should be scrapped until” the origin of eukaryotes is better understood, Dolan says.

But Pace says he has enough information to justify relegating prokaryote to the history books. “It’s got to go!” he says. “It’s intellectually no longer tenable.”

Click to view a larger version of the diagram.

Back Story | what’s in a tree?
The evolutionary history of life is at the heart of the debate over whether to continue using the term prokaryote (an umbrella term for the bacteria and archaea domains) or to shelve it. Different views of the origin of eukaryotes might influence the debate.

Three-domain tree
This tree is built on differences in rRNA genes and establishes bacteria, archaea and eukaryotes as separate domains of life with a common root. Norman Pace favors this tree, arguing against prokaryote because eukaryotes, bacteria and archaea originated at the same time, he contends.

Eocyte tree
Comparisons of many different genes give a different picture of the origin of eukaryotes. This tree shows eukaryotes branching off from a group of archaea known as eocytes. This arrangement might favor the use of prokaryote, since archaea preceded eukaryotes.

Web of life
Copious amounts of DNA transfer among organisms in all the domains has led to the idea that life is a web rather than a tree. In this scenario, there is no single common root.

Ring of life
UCLA’s James Lake found that eukaryotes have two types of genes — one set shared with archaea and another with bacteria. His “tree” organizes life like a ring, with the fusion of bacteria and archaea producing the eukaryotes.

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