Oceans of Archaea Abundant Oceanic Crenarchaeota Appear to Derive from Thermophilic Ancestors That Invaded Low-Temperature Marine Environments
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Oceans of Archaea Abundant oceanic Crenarchaeota appear to derive from thermophilic ancestors that invaded low-temperature marine environments Edward F. DeLong arth’s microbiota is remarkably per- karyotes), Archaea, and Bacteria. Although al- vasive, thriving at extremely high ternative taxonomic schemes have been recently temperature, low and high pH, high proposed, whole-genome and other analyses E salinity, and low water availability. tend to support Woese’s three-domain concept. One lineage of microbial life in par- Well-known and cultivated archaea generally ticular, the Archaea, is especially adept at ex- fall into several major phenotypic groupings: ploiting environmental extremes. Despite their these include extreme halophiles, methanogens, success in these challenging habitats, the Ar- and extreme thermophiles and thermoacido- chaea may now also be viewed as a philes. Early on, extremely halo- cosmopolitan lot. These microbes philic archaea (haloarchaea) were exist in a wide variety of terres- first noticed as bright-red colonies trial, freshwater, and marine habi- Archaea exist in growing on salted fish or hides. tats, sometimes in very high abun- a wide variety For many years, halophilic isolates dance. The oceanic Marine Group of terrestrial, from salterns, salt deposits, and I Crenarchaeota, for example, ri- freshwater, and landlocked seas provided excellent val total bacterial biomass in wa- marine habitats, model systems for studying adap- ters below 100 m. These wide- tations to high salinity. It was only spread Archaea appear to derive sometimes in much later, however, that it was from thermophilic ancestors that very high realized that these salt-loving invaded diverse low-temperature abundance “bacteria” are actually members environments. Novel cultivation of the domain Archaea. strategies, in situ biochemical and Another major archaeal group, geochemical methods, and environmental genom- the strictly anaerobic methanogenic archaea, ics promise to further our understanding of these produce most of the methane in our atmosphere. and other ubiquitous and abundant Archaea. Methanogens are one of the most cosmopolitan of cultivated archaeal groups, occupying diverse habitats that include anoxic sediments and rice Brief Overview of Archaea paddies, the rumen of cattle, the guts of termites, In the late 1970s, Carl Woese at the University hydrothermal vents, and deep subterranean of Illinois, Urbana-Champaign, and his collabo- habitats. A third phenotypic group of cultured rators, through their ribosomal RNA analyses, Archaea are the heat- and acid-loving thermo- first recognized Archaea as one of three major philes and thermoacidophiles. These unusual monophyletic lineages on Earth. Their analyses Archaea dwell at hydrothermal vents, hot Edward F. DeLong of several microbial groups, including extreme springs, deep subterranean environments, oil is a senior scientist halophiles and methanogens, revealed a unique reservoirs, and even on burning coal refuse piles. at the Monterey prokaryotic lineage that diverges from most fa- Cultivated members within one kingdom of Bay Aquarium Re- miliar bacterial groups at the deepest phyloge- the domain Archaea, the Crenarchaeota (Fig. 1), search Institute, netic levels. In recognizing the Archaea as a consist entirely of thermophilic species. Re- Moss Landing, separate evolutionary unit, Woese reclassified markably, a recent report by Derek Lovely at the Calif., delong@mbari organisms into three domains: Eucarya (all eu- University of Massachusetts, Amherst, suggests .org. Volume 69, Number 10, 2003 / ASM News Y 503 FIGURE 1 surveys of mixed microbial popula- tions from open ocean and coastal ma- rine waters. From such studies, Jed Fuhrman of University of Southern California in Los Angeles presented evidence in 1992 for one new type of archaeal ri- bosomal RNA sequence, recovered from planktonic microbes at depths of 500 m in the Pacific Ocean. At about the same time, I reported the discovery of two archaeal groups in coastal sea- water, one identical to that found by Fuhrman (the Group I planktonic Cre- narchaeota, Fig. 1), and an additional group (Group II planktonic Eur- yarchaeota, Fig. 1) distantly related to halophiles and methanogens (Fig. 1). We found that these Archaea contrib- Schematic tree showing the relationships of the four major groups of planktonic marine ute significantly to the total extractable Archaea relative to cultivated groups. rRNA in marine surface waters. The surprise at that time was that any Archaea could be found in cold, that some Crenarchaeota can grow at tempera- aerobic habitats of coastal and open ocean wa- tures exceeding 120°C (see p. 484). In addition ters. No cultivated, characterized Archaea were to high-temperature growth, some archaeal then known to grow at the salinities, tempera- thermophiles like Picrophilus oshimae also tures, and oxygen concentrations found in tem- thrive at extremely low pH, growing best at perate oceanic waters, shallow or deep. Soon, hydrogen ion concentrations approaching 1 M. researchers were reporting finding rRNAs be- longing to divergent archaeal groups in all sorts of habitats, including soils, freshwater and ma- Archaeal Ubiquity? rine sediments, and anaerobic digestors. Many Despite expanding information on cultivated of the new, nonmarine archaeal types in soils Archaea, only a small fraction of naturally oc- and freshwater sediments were related to the curring archaeal diversity is currently repre- marine Group I Crenarchaeota. Recently, a sur- sented in culture collections. Cultivation-inde- vey of the Great Lakes by Randall Hicks and pendent survey approaches pioneered by colleagues at the University of Minnesota, Du- Norman Pace of the University of Colorado, luth, has also revealed the prevalence of similar Boulder, have greatly expanded our current ap- types of Crenarchaeota. It has been surprising to preciation of natural microbial diversity. Such realize that Archaea, initially thought to be rel- surveys indicate that a significant amount of egated to extreme environments, actually thrive microbial diversity found in natural habitats has all over our planet, including the vast world so far eluded cultivation in the laboratory. Char- oceans, the Great Lakes, and the very soil be- acterizing these elusive and understudied but neath our feet. ubiquitous microorganisms remains a critical Among the four major groups of planktonic goal for gaining a deeper and truer appreciation marine Archaea, the most abundant appear to of microbial evolution, physiology, and ecology. be the first groups recognized, Group I Crenar- Although Archaea were thought to preferen- chaeota and Group II Euryarchaeota (Fig. 1). tially occupy environments that are inhospitable Two other planktonic archaeal groups have also to Eucarya and Bacteria, their ecological and been detected, but appear to be lower in abun- physiological diversity turns out to be far greater dance, according to recent surveys. The Group than previously supposed. Some early hints III planktonic Archaea, found in waters below came from PCR-based, ribosomal RNA-gene the photic zone, are peripherally related to the 504 Y ASM News / Volume 69, Number 10, 2003 Breaking the Ice, Finding New Habitats for Archaea Marine biologist Edward DeLong around the boat, and nothing lone, scuba received an unforgettable lesson budged. Fortunately, the situation dive, and pad- about eight years ago during a wasn’t dire, but it was unlikely dle a kayak. field trip to Antarctica, when the that another icebreaker would be “I fell in love ship he was on became lodged in available to dislodge them. So with the ice. What ordinarily should have they waited, wondering whether ocean as a been a four-day journey from they would have to remain there kid. I really South America to Antarctica until the summer thaw. do love the stretched into two weeks with no When a shift in the winds led sea,” he says. rescue in sight. “When you’re the ice to break up, they were free “I always tell people that it’s down in Antarctica, nature calls but also low on fuel. They had to amazing I get paid to do what I the shots and you learn to be turn back, refuel, and start again. do.” adaptable,” says DeLong, a senior “It wasn’t scary, just an interest- After finishing high school, De- scientist with the Monterey Bay ing experience in sociology, to see Long moved to Alaska for a year Aquarium Research Institute in how you and your colleagues “to find myself,” then returned to Moss Landing, Calif. adapt to being stuck on a boat for California to start college. He DeLong and his colleagues two weeks with nothing to do,” studied biology at Santa Rosa were en route to the Antarctica Delong says. “Actually, it was Junior College, Calif., in 1980, Peninsula in August 1995, the fun.” before obtaining a B.S. degree in austral winter, to study Archaea, DeLong has been having fun bacteriology from the University then newly discovered to inhabit for his entire career. It began of California, Davis (UCD) in cold-ocean waters. They were during his childhood with a love 1982, and a Ph.D. in marine biol- traveling by icebreaker, but that of the sea. Delong, now 45, ogy from the Scripps Institute of didn’t prevent the ship from get- grew up in Sonoma, Calif., where Oceanography, San Diego, Calif., ting trapped in the ice. Ice formed he learned to skin dive for aba- in 1986. In 1989, he received an Continued order Thermoplasmatales. Members of the pe- archaeal rRNA in marine plankton yielded some lagic Group IV Archaea, discovered by Fran- unexpected surprises. Perhaps most startling was cisco Rodriguez-Valera and collaborators of the the high relative abundance of Archaea in winter Universidad Miguel Hernandez in Spain, appear surface waters off Antarctica, where planktonic to be related to haloarchaea, and apparently Crenarchaeota sometimes comprise as much as inhabit deep ocean waters. Currently, hundreds 20% of total microbial rRNA. Those coastal of ribosomal RNA sequences derived from ma- waters are Ϫ1.8oC, a far cry from the 80oCor rine planktonic Archaea exist in the public da- higher growth temperature optima of cultivated tabases.