or collective redistirbution other or collective or means this reposting, of machine, is by photocopy article only anypermitted of with portion the approval Th of society. send allcorrespondence oceanography to: e [email protected] or usA. md 20849-1931, society, rockville, po box 1931, e oceanography Th Th in published been has is article speciAL issue feAture Oceanography , Volume 1, a quarterly 20, Number Th journal of society. oceanography copyright e 2007 by society. epermissionreserved. oceanography Allrights is grantedTh use in to copy teaching research. and for article this republication, systemmaticreproduction,

Th e emergence of on earth by mitcheLL schuLte

42 Oceanography Vol. 20, No. 1 AmoNg the most enduring and perplexing questions pondered by humankind are why, how, and when life began on Earth, and whether life exists elsewhere in the solar system or the universe. Attempts to answer these questions have fallen under the purview of a number of areas of inquiry, including philosophy, religion, and, more recently, dedicated scientifi c inquiry. Scien- tifi c study of life’s beginnings necessarily draws from a wide variety of disciplines. Because of the complexity of the problem, geologists, chemists, biologists, and physicists, as well as engineers and Th e emergence of mathematicians, have all been involved in origin-of-life research. Geologic evidence indicative of biological processes dates back to around 3.8–3.5 billion years ago. Features that resemble modern are present as microfossils in 3.5-billion-year- old rocks in Australia and are thought by some to show that life was well developed by that time. Life on earth Carbon found in metamorphosed rocks from Akilia Island, Greenland, is isotopically light, thought by many to demonstrate that organisms were fractionating carbon isotopes 3.8 billion years ago. Much of the fossil and chemical evidence once thought with certainty to be products of biologi- cal activity has been questioned recently, however, and a defi nitive time frame for life’s beginnings remains controversial (Chyba and Hand, 2005). Regardless of exactly when life fi rst appeared, Earth was very different at the time than it is at present. The early Earth was a violent place, with rem- nants of the solar system’s formation colliding with its surface frequently until around 3.8 billion years ago. Many of the collisions would have been of suffi cient force to heat the oceans to tem- peratures above 100°C, and even to vaporize them on occasion1. In fact, the oceans are thought to have maintained temperatures as high as 70–100°C for much of Earth’s early history (Robert and Chaussidon, 2006), due in part to the atmospheric composition. The atmosphere contained no oxygen (oxygenic photosynthesis had yet to develop), and could have contained up to 10–100 bars of carbon dioxide, which would have warmed Earth’s surface and caused the oceans to be acidic (Nisbet and Sleep, 2001; Russell et al., 2005). Earth’s interior was hotter than at present due to friction from collisions, higher radioactive decay, and remnant frictional heat from its formation. Because of the high heat fl ow, volcanic and hydrothermal activity on the early Earth would have been greater than at present. It was under these geological conditions that life made its debut.

1 Th e collision of the earth with a particularly large body, roughly the size of mars, ~ 4.4 billion years ago resulted in melting of the earth and the formation of the moon.

Oceanography march 2007 43 Life in Extreme water activity. Nonetheless, organisms however, and contend that thermophily Environments living at high temperatures, like those may simply represent an adaptation to The discovery in 1977 of hydrothermal found at deep-sea hydrothermal black survive the violent nature of the early systems at a seafloor spreading cen- smoker chimneys (see article by Fisher Earth (Forterre, 1998; Galtier et al., 1999; ter near the Galápagos Islands pro- et al., this issue), are some of the most Miller, 1998). vided new direction and revolutionized extraordinary examples. The current Other clues from the convergence of “origin-of-life” studies (Corliss et al., record holder for high-temperature life biology and hydrothermal geochemistry 1979). The abundance and diversity of is a known as Strain 121 support a hydrothermal origin of life. animals and microorganisms found in (tentatively named barossii) First, there are structural and composi- the dark depths of the seafloor near the for its ability to grow at a temperature tional resemblances between iron-sulfur hydrothermal vents, far removed from of 121°C2 (Kashefi and Lovley, 2001; minerals that form routinely during hy- the direct influence of the sun’s energy Lovley et al., 2004). Strain 121 was iso- drothermal processes and the iron-sulfur (although the animals at hydrother- lated from a chimney centers of electron transfer proteins that mal vents do require oxygen, originally recovered from the Endeavour Segment are part of the core of many produced through photosynthesis and of the Juan de Fuca mid-ocean ridge, organisms (ferrodoxins) (Russell et al., extracted from seawater), naturally ~ 2200 m below sea level off the Pacific 2005). Second, the abundance of sulfur- attracted a great number of researchers northwest coast of North America. On- bearing minerals in hydrothermal sys- to study the nature of the life in such a going research in extreme environments tems could have supported sulfur-based seemingly inhospitable environment. continues to broaden our view of habit- that are common energy While the animals include unique but ability on the early Earth and through- sources for primitive chemolithotrophic somewhat familiar forms, the microor- out the solar system. microorganisms (i.e., those that use in- ganisms inhabiting seafloor hydrother- What can these modern organisms organic chemicals as an energy source). mal systems are unusual and demon- tell us about how life began, and the The connection between early life and strate a remarkable ability not only to nature of early life on Earth? Accord- sulfur chemistry is reinforced by the tolerate such challenging environments, ing to comparisons of sequences of the reliance of biology on a variety of sulfur- but to thrive in, and in fact require, these 16S rRNA gene (Figure 1), prokaryotic bearing organic compounds, including conditions. These organisms, dubbed organisms (single-celled and essential enzymes, amino acids, and pro- “” for their ability to toler- that lack a nuclear membrane) teins (Schulte and Rogers, 2004). Finally, ate extremes in environmental condi- exhibiting the most primitive character- hydrothermal systems have very likely tions, exhibit a vast diversity of metabo- istics are all thermophilic (heat-loving), operated continuously on Earth since lisms and inhabit niches that were once with optimal growth temperatures above the establishment of its oceans. Their considered unsuitable for life. Our cur- 60°C. This observation suggests that the existence beneath the ocean’s surface rent understanding of extreme habitats “last common ancestor” to all life cur- would have provided safe haven for in- extends to conditions of extreme pH rently on Earth was an organism (or cipient life, protecting it from changing (< 2 and > 10), pressure (from surviv- community of organisms) that lived at solar, atmospheric, and surface condi- ing the vacuum of space to the deepest high temperature. This result, coupled to tions as Earth evolved. Thus, these sys- submarine trenches), metal content, the fact that volcanic and hydrothermal tems would have been a reliable source salinity, alkalinity, radiation, and low activity were greater on the early Earth of geochemical energy for over four bil- has led to the widely accepted hypoth- lion years (Shock et al., 1998). In addi- Mitchell Schulte (schultemd@ esis that life began under hydrothermal tion, they provide a natural mechanism missouri.edu) is Assistant Professor, Depart- conditions. Other researchers disagree, for concentrating energy and chemicals, ment of Geological Sciences, University of Missouri, Columbia, MO, USA. 2 Strain 121 has been shown to tolerate temperatures as high as 130°C, but is not capable of growth at that temperature.

44 Oceanography Vol. 20, No. 1 Eukarya

Microsporidia Euglena Animals Plants Fungi Ciliates Slime Diplomonads molds

Green nonsulfur bacteria Bacteria

Gram + Sulfolobus Proteobacteria Thermotoga Thermofilum Cyano- Thermoproteus Archaea Flavobacteria bacteria Pyro- dictium Thermococcus Methanobacterium Green sulfur bacteria Archaeoglobus Last Common Ancestor Euryarchaeota

Figure 1. The universal tree of life, showing the three domains, based on comparison of the ribosomal RNA gene. The lengths of individual line seg- ments indicate the evolutionary distance in terms of the number of changes in the genetic sequence from one organism to another. The segments in red indicate thermophilic organisms; note that they cluster near the base of the tree, implying that the last common ancestor of extant life was thermophilic. After Woese et al. (1990)

especially trace metals (e.g., molybde- Earth include carbon dioxide and oxi- dioxide, one of the most abundant vol- num, zinc, tungsten, cobalt) that are es- dized forms of iron that may have been canic gases, as their source of carbon. sential for proper enzyme function, in- generated photochemically). Many of the Indeed, shortly after the first discovery cluding those found in . organisms with “primitive characteris- of deep-sea hydrothermal vent fields, Whatever the nature of the condi- tics” are lithotrophs that metabolize the Corliss et al. (1981) and Baross and tions under which life began, it is clear inorganic chemicals found in abundance Hoffman (1985) suggested that the con- that it was necessary to have a source of in volcanic and hydrothermal environ- stant supply of energy from geochemical metabolic energy, which requires both ments (such as hydrogen and hydrogen reactions on the early Earth might have electron donors (such as hydrogen and sulfide). Most are also autotrophs, mean- provided the perfect circumstances for hydrogen sulfide) and electron accep- ing that they are able to synthesize their life to develop. tors (reasonable candidates for the early own organic matter starting with carbon

Oceanography March 2007 45 Abiotic Sources of (i.e., composed of large concentrations Some claim that these environments are Organic Compounds of methane and ammonia), but instead simply too hot for organic molecules to Because life on Earth is primarily consisted of a mixture of substantial survive (Miller and Bada, 1988; Miller carbon-based, identifying sources of pre- amounts of carbon dioxide and dinitro- and Lazcano, 1995; White, 1984). These biotic organic compounds on the early gen gases. Attempts to repeat the Miller- arguments are countered by theoretical Earth is a key element to understand- Urey experiment with these gases have (Shock and Schulte, 1998) and experi- ing the emergence of life. The famous yielded little, if any, “interesting” organic mental (Seewald, 1994; Seewald et al., Miller-Urey experiment (Miller, 1953, compounds (Chyba and Hand, 2005). 2006) evidence that demonstrates the 1955; Miller and Urey, 1959) demon- Suggestions for other sources of or- formation and stability of organic com- strated for the first time that organic ganic material that may have been avail- pounds at relatively high temperatures molecules essential for life could be gen- able to incipient life include carbona- given the right geochemical conditions. erated from strictly abiotic constituents. ceous chondrite meteorites and comets. Measurements of deep-sea hydrothermal In their experiments, Miller and Urey Carbonaceous chondrites contain up to fluids also show that methane and other started with methane and ammonia 10 wt.% carbon, primarily in a complex light hydrocarbons have a probable abi- gases. Energy in the form of electrical aromatic structure. Up to 600 ppm of otic origin (Holm and Charlou, 2001). sparks, representing lightning discharges, carbon are found in the form of soluble Other abiotically produced organic com- facilitated chemical reactions to generate organic compounds such as carboxylic pounds in these fluids are predicted to a variety of organic compounds, includ- acids, ketones, alcohols, and even amino occur, but have not been studied to date. ing amino acids, in a tarry matrix. As acids (Cronin, 1998). Studies show that Among the organic compounds pre- amino acids are the primary components these materials frequently survive the dicted to form during fluid mixing of of proteins, the most versatile and es- journey through Earth’s atmosphere hydrothermal vent fluids and seawater sential biological macromolecules, many and are delivered intact to the surface. are long-chained carboxylic acids (Shock scientists thought it would be a simple Whether they could then be concen- and Schulte, 1998). Aggregates of these step to decipher the origin of living sys- trated and react to form more complex molecules can develop into spherical tems through polymerization of these molecules remains an open question. structures called micelles. Micelles have smaller molecules. However, despite However, meteorites and comets would an outer surface that is composed of the this early success, the processes through have been a significant source of raw ma- nonpolar, hydrophobic portion of long- which life developed from simple organ- terials, like carbon and nitrogen. chained carboxylic acids, which excludes ic molecules into systems that use encap- Hydrothermal systems have also been aqueous fluids and chemicals from the sulating membranes and pass informa- proposed as locations where organic interior. The polar, hydrophilic ends of tion to succeeding generations remains compounds could have been synthesized these molecules point toward the inte- to be solved. In addition, the relevance on the early Earth. Experimental work riors of the micelles, forming a charged of the starting materials used by Miller has demonstrated that organic com- surface that can attract ionic species. and Urey in their experiment has been pounds like amino and carboxylic acids This structure can maintain a separation called into question. At the time, Miller can be formed under hydrothermal con- of charge and a redox gradient, similar to and Urey thought, by extrapolation from ditions. In some of these experiments, re- the way modern organisms’ cells operate the composition of Jupiter’s presumably actions on the surfaces of sulfur-bearing and could have been the primitive mem- primitive atmosphere, that methane and minerals involving inorganic forms of branes that allowed life to develop. ammonia represented major constituents sulfur and carbon provide the energy to Alternatively, Michael Russell and his of Earth’s early atmosphere. While the convert carbon dioxide or carbon mon- colleagues at the University of Glasgow nature of the early Earth’s atmosphere oxide into organic matter (Cody et al., (Russell et al., 2005) speculate that iron- is not certain, geological evidence sug- 2000; Heinen and Lauwers, 1996; Hennet sulfur minerals that form hollow, spheri- gests that it was not strongly reducing et al., 1992; Wächtershäuser, 1988). cal structures may have served as tem-

46 Oceanography Vol. 20, No. 1 plates for the first cells. These structures as a possible site for extraterrestrial life. type chemistry. Because methane would were shown to develop during experi- Tales of martians invading Earth aside, be quickly photooxidized by ultraviolet ments in which alkaline hydrothermal factors that make Mars a plausible site for light from the sun, finding even these fluids are mixed with acidic solutions life include its compositional similarity to concentrations of methane means that it thought to represent the early oceans. Earth and abundant evidence for liquid is being actively generated. On Mars, the Similar structures are seen in more mod- water at its surface some time in its early observed methane could be coming from ern sulfide deposits that form as mounds history. No evidence of life has yet been reactions between subsurface fluids and during hydrothermal generation of ore found at the surface of Mars. It could be ultramafic minerals (Schulte et al., 2006). bodies. Russell et al. (2005) speculate that we have simply not looked in the Alternatively, it is possible that the meth- that these hydrothermally produced sul- right place. The other possibility is that ane is being produced by methanogenic fide mounds formed in abundance on any extinct or extant martian life must (methane-producing) microorganisms the early Earth due to disequilibrium be contained in the subsurface. Such life living in the subsurface. between the oceans and the hydrother- would likely be similar to chemotrophic Europa, one of the Galilean satellites mal fluid. The sulfide minerals served as life on Earth that feeds on geochemical of Jupiter, has recently become another catalytic surfaces where carbon dioxide rather than photosynthetic energy. very attractive target for researchers in- would be reduced to organic acids and The discovery of the Lost City hydro- terested in the possibility of life outside other organic compounds. In this view, thermal vent field near the Mid-Atlantic Earth. Beneath a thick ice layer, Europa the inorganic protomembranes thus Ridge may provide a glimpse into the has a 100-km-thick liquid water ocean formed were gradually replaced by the nature of life on Mars, if it exists (or ever that most likely covers a rocky mantle organic material being continually gen- existed). In the Lost City hydrothermal (Figure 2). The tidal pull of Jupiter pro- erated through hydrothermal circulation. vent field, chemical reactions between vides enough frictional heat to keep the the reduced ultramafic (high in magne- water liquid below the ice layer, and may Is There Life Beyond Earth? sium and iron) rocks and seawater pro- also provide enough heat to melt at least Because geology seems to be intricately duce very alkaline hydrothermal fluids some portion of the rocky mantle. This linked with life on this planet, the ques- (Kelley, 2005). These fluids react with heat availability could result in a situa- tion arises about whether there are other seawater to form carbonate chimneys as tion analogous to Earth’s hydrothermal Earth-like planets in the universe that well as abundant hydrogen and methane, systems, in which molten rock induces may have developed life. In addition, the which serve as very useful energy sources hydrothermal circulation through the planetary history of other planets and for in situ microbial communities. While crust, leading to water-rock interactions moons in our own solar system is simi- there are a number of types of hydro- that produce hydrothermal vent fluids. lar to that of Earth, leading to questions thermal systems present on Earth, early On Earth, the resulting fluids are out about the best possibilities for finding ex- in Earth’s history these would likely have of chemical and thermal equilibrium traterrestrial life close to home. Because been dominated by ultramafic rocks re- with the original seawater, providing life as we know it requires liquid water, acting with acidic fluids (Russell et al., energy sources for a great diversity of most of the effort has focused on those 2005). Similar systems also might have chemosynthetic microorganisms. Will planetary bodies displaying evidence of been present early in the history of Mars, we find similarly strange communities liquid water, either at present or at some especially in the subsurface, the most of microorganisms and animals in the time in the past. Most of the attention re- likely location for martian life (Russell depths of Europa’s ocean? Geochemical cently has focused on Mars, where NASA and Hall, 1999). Recent observations of modeling suggests that there is chemical has a vigorous research program; Europa, the martian atmosphere indeed indicate energy available to support a microbial one of the moons of Jupiter; and Titan, modest amounts of methane that appear community (McCollom, 1999), but only one of the moons of Saturn. to correspond with outcrops of the min- continued exploration will allow us to Mars has long commanded attention eral olivine, consistent with Lost City- answer this question.

Oceanography March 2007 47 Figure 2. Europa, one of Jupiter’s moons, has a liquid water ocean beneath its exterior ice shell, and a rocky mantle. Hydrothermal systems are postulated to exist at the interface between the ocean and mantle. Modified from a NASA illustration

Summary Origin-of-life research takes essen- forms of life to trace back the genetic Despite a great deal of advancement in tially two approaches to these issues. and metabolic nature of the first life. origin-of-life research, the steps that led One, called the “bottom-up” approach As an example, researchers have shown from chemistry to life remain elusive. (building life), addresses the formation that RNA is capable of catalyzing reac- Some of the outstanding issues that are of life starting with abiotic chemistry tions and storing genetic information. poorly understood include the selectiv- and trying to understand the chemical This observation led to the idea of an ity of molecules (why does life use only evolution that led to life. Recent research RNA world, in which RNA served both 22 protein-forming amino acids out along these lines has led to progress in roles, rather than the current situa- of over 70 amino acids?), the origin of addressing a number of these issues. For tion in which DNA and proteins share chirality (why does biology use only example, common rock-forming mineral these duties (Orgel, 2004). However, the “left-handed” amino acids but primarily surfaces appear to absorb certain organic chemistry that led to the development of “right-handed” sugars?), the role of min- molecules selectively, including amino RNA remains unexplained. In addition, eral surfaces in adsorbing organic mol- acids, and to absorb biological molecules molecular biology studies are unraveling ecules and serving as templates for fur- of a particular handedness (Hazen, the differences in genetic sequences of ther reaction, the formation of the first 2004). Minerals may thus have provided modern organisms that live in extreme membranes and encapsulation of chemi- a template for organizing life. environments, helping us decipher the cal reactions into cells, and the develop- The other approach is called “top way these organisms are able to use geo- ment of genetic information molecules down” (breaking down life). The idea chemical energy and therefore how they (RNA and DNA). is to use what we know about modern are related to Earth’s first life.

48 Oceanography Vol. 20, No. 1 Ultimately, both approaches are use- system: Meteorites. Pp. 119–146 in The Molecular life—did it occur at high temperatures? Journal of ful and necessary. Perhaps the combined Origins of Life. A. Brack, ed, Cambridge Univer- Molecular Evolution 41:689–692. sity Press, Cambridge, UK. Miller, S.L., and H.C. Urey. 1959. Organic com- efforts of all those studying the origins Forterre, P. 1998. Were our ancestors actually hyper- pound synthesis on the primitive Earth. Science of life will result in a more comprehen- thermophiles? Viewpoint of a devil’s advocate. 130:245–251. Pp. 137–146 in Thermophiles: The Keys to Mo- Nisbet, E.G., and N.H. Sleep. 2001. The habitat and sive understanding of the processes that lecular Evolution and the Origin of Life? J. Wie- nature of early life. Nature 409:1,083-1,091. led to the emergence of life on Earth, gel and M.W.W. Adams, eds, Taylor & Francis, Orgel, L.E. 2004. Prebiotic chemistry and the origin London, UK. of the RNA world. Critical Reviews of Biochemis- and will help us explore the solar system Galtier, N., N. Tourasse, and M. Gouy. 1999. A non- try and Molecular Biology 39:381–393. and beyond for evidence that we are not hyperthermophilic common ancestor to extant Robert, F., and M. Chaussidon. 2006. A palaeotem- alone. While continuing advances have life forms. Science 283:220–221. perature curve for the Precambrian oceans based Hazen, R.M. 2004. Chiral crystal faces of common on silicon isotopes in cherts. Nature 443:969–972. furthered our understanding of how rock-forming minerals. Pp. 137–151 in Progress Russell, M.J., and A.J. Hall. 1999. On the inevitable biology relates to abiotic processes, far in Biological Chiralty, G. Palyi, C. Zucchi, and L. emergence of life on Mars. Pp. 26–36 in The Caglioti, eds, Elsevier, New York. 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