CONFRONTING CLIMATE CHANGE A SIGMA XI REPORT : American Scientist MAYA–JUNEm 2007 ericTHE anMAGAZINE OF SIGMAS XIc, THEi SCIENTIFICen RESEARCHtis SOCIETYt American Scientist Volume 95 Number 3 Volume May–June 2007 A reprint from American Scientist the magazine of Sigma Xi, The Scientific Research Society This reprint is provided for personal and noncommercial use. For any other use, please send a request to Permissions, American Scientist, P.O. Box 13975, Research Triangle Park, NC, 27709, U.S.A., or by electronic mail to [email protected]. ©Sigma Xi, The Scientific Research Society and other rightsholders Extreme Microbes Salt-loving microorganisms are helping biologists understand the unifying features of life and molecular secrets of survival under extreme conditions Shiladitya DasSarma een from the air, the irregular grid the microscopic world in a drop of near- Sof evaporation ponds at the south saturated brine contains a menagerie of end of San Francisco Bay in Califor- bizarre life forms that defy these con- nia is a kaleidoscopic quilt of reds and ventions. Unlike the extremophiles that purples. These ponds take their col- have adapted to a single extreme condi- ors from the single-celled microorgan- tion, haloarchaea are metabolically ver- isms that live there, strange beings that satile. They can grow aerobically (with thrive in concentrated salt solutions. oxygen), anaerobically (in the absence Such extreme conditions kill almost of oxygen) or phototrophically (using every form of life on the planet, but not light energy), and can adapt to fluctua- the salt-loving archaea. They are mem- tions in temperature, pH and metal-ion bers of an ancient kingdom that exist- concentration. They are resistant to des- ed even before Earth had an oxygen at- iccation, sunlight and ionizing radiation. mosphere. The fact that many archaea As a result, they can be found in anoxic live under impossible circumstances— salt marshes, hydrothermal vents, pe- boiling temperatures, lethal radia- rennially frozen Antarctica and pockets tion, near-complete desiccation—has of brine deep underground and under led scientists to dub them “extremo- the seafloor. philes.” These organisms may even be The biggest hurdle to studying most capable of hitchhiking through space. species of archaea is recreating in the As human beings, our intuitive con- laboratory the extreme conditions cept of life is influenced by the visible they need. By contrast, the salt-lov- biosphere—temperate terrestrial, fresh- ing haloarchaea are easily cultivated, water and marine environments. But and microbiologists have used them in molecular, genetic and physiological Shiladitya DasSarma received his Ph.D. in biochem- experiments. Haloarchaea grow best istry in 1984 from the Massachusetts Institute of under hypersaline conditions, from Technology and then took up a two-year postdoctoral slightly concentrated seawater to near- fellowship at Massachusetts General Hospital and saturated brine. These attributes, plus Harvard Medical School. He served on the faculty the availability of genomic data and Figure 1. In places where salty brine is evap- of the University of Massachusetts-Amherst from orated to harvest its dissolved minerals, such tools for molecular manipulation, have 1986 to 2001. In 2001, he moved his laboratory to as Lac Rose (“Pink Lake”) in Senegal, the the Center of Marine Biotechnology at the Univer- elevated them to the status of “model” evaporation ponds or salterns take on oth- sity of Maryland Biotechnology Institute, where he organisms that shed light on other ex- is a full professor. He also holds a teaching appoint- tremophiles, including other archaea bacteria and those evolutionary relics ment in the Graduate Program in Life Sciences at and even higher organisms. called archaea. Although the two look the University of Maryland-Baltimore. His labora- the same under the microscope, archaea tory group includes his wife, Priya DasSarma, who Diversity and Unity have molecular characteristics that are earned her M.S. in microbiology from the University Until the 1970s, scientists believed that more similar to nucleus-containing of Massachusetts with a certification to teach biol- all prokaryotes—those single-celled mi- eukaryotes—organisms such as yeasts, ogy. She currently specializes in biotechnology edu- croorganisms that lack a nucleus—were plants and animals. These traits confirm cation and science outreach for students of all ages. Writing on page 230, she discusses the advantages “bacteria.” The pioneering work of Carl that archaea are fundamentally distinct of Halobacterium NRC-1 as a classroom tool. Ad- Woese at the University of Illinois at from bacteria. dress: University of Maryland Biotechnology Insti- Urbana-Champaign, and his colleagues Such distinctions notwithstand- tute, 701 East Pratt Street, Baltimore, MD 21202. proved otherwise. Today, prokaryotes ing, scientists using haloarchaea have Internet: [email protected] are divided into two groups: the “true” made several landmark findings © 2007 Sigma Xi, The Scientific Research Society. Reproduction 224 American Scientist, Volume 95 with permission only. Contact [email protected]. Ron Giling/Peter Arnold, Inc. erworldly hues. The colors—oranges, reds, pinks and purples—come from halophilic microorganisms, which thrive under such forbidding conditions. As a result of an evolutionary history filled with genetic swaps with other microbes, haloarchaea can withstand not only high con- centrations of salt but also extremes of temperature, pH and solar radiation. Such traits make them candidates for interplanetary travel, locked away in salty capsules within meteoric chunks of rock. that have wider implications for mi- Another early discovery first made a mill wheel harnesses the current of crobial and multicellular life forms. in haloarchaea was the protein bac- a river to do useful work. In archaea, For example, evidence from haloar- teriorhodopsin. First identified by the purple-tinted bacteriorhodop- chaea helped H. Gobind Khorana at Walther Stoeckenius of the University sin proteins cluster in a specialized MIT (with whom I began my studies of California, San Francisco, bacterio- region of the cell surface called the of haloarchaea) to establish the stan- rhodopsin uses photons of sunlight purple membrane, where they enable dard genetic code—the Rosetta Stone to pump hydrogen ions (protons) out the harvest of light energy for growth of biology that allows the information of the cell. This action creates a polar- under conditions where oxygen is in genes to be used as a blueprint for ized cell membrane. A separate pro- scarce. In classic experiments, Stoeck- proteins. The existence of this code is tein complex harnesses the flow of enius and others showed that light one of the strongest lines of evidence protons trying to reenter the cell to could drive the synthesis of adenos- for the unity of all life on our planet. provide energy—similar to the way ine triphosphate or ATP—the cellular © 2007 Sigma Xi, The Scientific Research Society. Reproduction www.americanscientist.org 2007 May–June 225 with permission only. Contact [email protected]. marine Extreme Genomics cyanobacteria Halobacterium NRC-1 100 Despite its name (more on this later), an organism that was known as “Halobacte- rium species NRC-1” was the first halo- archaeon—and one of the first archaea of any kind—to have its genome studied. W. Ford Doolittle at Dalhousie Univer- sity and my research group (then at the University of Massachusetts Amherst) conducted those early experiments. NRC-1 is in most respects a typical halo- archaeon, widely distributed in hyper- growth rate (percent) saline environments such as the Great saturation seawater Salt Lake. The genome of this species has 0 0 1 2 3 4 5 the unusual property of being spontane- ously unstable, such that entire physio- sodium chloride (moles per liter) logical systems, such as the phototrophic purple membrane and buoyant gas-filled vesicles, are sometimes mutated. This cu- Figure 2. Normal seawater has around 30 grams of sodium chloride (0.5 mole) per liter (left), riosity led us to identify a large number a concentration that supports cyanobacteria, sometimes called blue-green algae. By contrast, of mobile genetic elements—similar to Halobacterium NRC-1 thrives in brine that is roughly eight times saltier. This concentration the “jumping genes” described by pio- borders the saturation point—the point at which solid salt begins falling out of solution. Seen neering geneticist Barbara McClintock in a transmission electron micrograph (right), the gas-filled sacs that buoy NRC-1 cells into the sunlight look like the holes in Swiss cheese. (Micrograph courtesy of the author.) in maize. These elements were the first to be discovered in any archaeon. We also found that NRC-1 carries a pair of smaller DNA molecules alongside its chromosome. The sequence of the NRC-1 genome was completed in the summer of 2000. light It was the first complete genome to be hydrogen ions sequenced with funds from the U.S. National Science Foundation. The ge- nome consists of a large, circular chro- mosome (2,014 kilobases) and the two smaller DNA hoops, called plasmids or replicons: pNRC100 (191 kilobases) and pNRC200 (365 kilobases). The pNRC replicons contain many of the DNA repeats that enable genomic rear- rangements, including 69 of 91 mobile elements, 33 to 39 kilobases of so-called bacteriorhodopsin ADP inverted repeats, which can flip or in- vert portions of the circles, and 145 ki- P lobases