Microbe understudies await their turn in the ecosystem limelight

On the marine microbial stage, there appears to be a vast, varied group of understudies only too ready to step in when “star” microbes “break a leg.”

At least that’s what happens at the Lost City hydrothermal vent field, according to research results published this week in the journal Proceedings of the National Academy of Science (PNAS).

The Lost City hydrothermal vent field is located in the mid-Atlantic and is the only one of its kind found thus far. It offers scientists access to microorganisms living in vents that range in age from those newly formed to those tens of thousands of years old.

A bit-player among microbes found in scant numbers in younger, more active vents became the lead actor in a chimney more than 1,000 years old where venting had moderated and cooled, changing the ecosystem, according to Phillip Taylor of the National Science Foundation (NSF)’s Division of Ocean Sciences, which funded the research.

This is the first evidence that microorganisms can remain rare for such a long time before completely turning the tables to become dominant when ecosystems change, says William Brazelton, a University of Washington (UW) postdoctoral researcher. It seems logical, but until recently, scientists weren’t able to detect microorganisms at such low abundance, he says.

In 2006, scientists led by Mitchell Sogin of the Marine Biological Laboratory in Woods Hole, Mass., and a co-author of this week’s paper, published the first results showing that microorganisms in the marine environment had been woefully undercounted.

Using the latest DNA sequencing techniques, they found that marine microorganisms could be 10 to 100 times more diverse than previously thought.

The scientists coined the term “rare biosphere” to describe a vast but unrecognized group of microorganisms–“rare” because each individual type of microorganism appeared to be present in only very low numbers, so low that they were previously undetectable.

If the new way of determining microbial diversity was accurate, scientists were left to wonder why such a large collection of low-abundance organisms existed.

“A fundamental prediction of the ‘rare biosphere’ model is that when environmental conditions change, some of these rare, preadapted microbes can rapidly exploit the new conditions, increase in abundance, and out-compete the once abundant organisms adapted to past conditions,” Brazelton and co-authors write in their paper.

Yet, they continued, “No studies have tested this prediction by examining a shift in species composition involving extremely rare taxa occurring during a known time interval.”

Until now.

Lost City, discovered by University of Washington researcher Deborah Kelley and others during an NSF expedition in 2000, was named in part because it was discovered by scientists using the research vessel Atlantis.

Follow-up work by Kelley and others showed that the hot springs are formed in a very different way than the metal-rich black smoker vents scientists have known about since the 1970s.

Unlike the 700 degrees Fahrenheit black smokers, the chimneys, vents and other structures at Lost City are nearly pure carbonate, the same material as limestone in caves. They’re formed by serpentinization reactions, a chemical reaction between seawater and mantle rocks that underlie the field.

Water venting at Lost City is generally at 200 F or less. The fluids are highly alkaline and enriched in the gases methane and hydrogen–important energy sources for the microbes that inhabit Lost City.

Lost City also differs from magma-driven hydrothermal systems in that it is very long-lived.

There have been numerous seasonal and short-term studies of microbial responses to environmental changes–lasting years at the most–the Lost City hydrothermal vent field has provided a way to look at changes in vent ecosystems 1,000 years apart in age.

Analyses by Brazelton and colleagues revealed that DNA sequences that were rare in younger vents were abundant in older ones. Because it is likely that the older Lost City chimneys released higher-temperature, higher-pH fluids when they were younger, as the ecosystem changed, the rare microorganisms came to the fore.

This round of near-disappearance then dominance could have happened repeatedly during the more than 30,000 year lifetime of the Lost City vent field. The microorganisms present today are “pre-adapted” to certain conditions–and are waiting for the ecosystem to change to suit them best.

“The rare biosphere of the Lost City microbial community represents a large repository of genetic memory created during a long history of past environmental changes,” the authors write. “The rare organisms were able to rapidly exploit the new niches as they arose because they had been previously selected for the same conditions in the past.”

The work was funded by the NSF, NASA and the W.M. Keck Foundation.

Authors of the paper are William Brazelton, Deborah Kelley and John Baross, UW; Mitchell Sogin, Marine Biological Laboratory at Woods Hole; Chuan-Chou Shen, National Taiwan University, Taipei; Lawrence Edwards, University of Minnesota; and Kristin Ludwig, Consortium for Ocean Leadership, Washington DC.

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