PerspectiveOcean Science

Lost City Life

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Science  04 Mar 2005:
Vol. 307, Issue 5714, pp. 1420-1422
DOI: 10.1126/science.1109849

One of the first underwater scenes in James Cameron's spectacular new IMAX adventure Aliens of the Deep stars a truly alien panorama. It is a stunning view of the giant white carbonate chimneys of a submarine hydrothermal vent field called Lost City, which looms like a conglomeration of colossal beehives from outer space. The discovery of the Lost City hydrothermal field in December 2000 was a real fluke (1). A team of scientists working with Deborah Kelley came across this new ecosystem during an off-axis camera survey near the Mid-Atlantic Ridge at 30°N. As Kelley et al. (2) report on page 1428 of this issue, they returned in 2003 for a detailed study of Lost City and discovered a remarkable array of micro- and macro-organisms that reside in this hydrothermal ecosystem, which is fueled by abiotic methane and hydrogen. Their results provide fascinating insights into the nature of life at Lost City. Although Lost City represents a unique vent system, the underlying processes responsible for its formation and geochemical setting are likely to drive many other vent ecosystems. This has important implications for biogeochemical cycles, for ocean exploration, and for understanding microbial habitats on Earth and beyond.

The Lost City vent field is characterized by carbonate towers up to 60 m in height. It is located on 1.5-million-year-old rock that is 15 km away from the spreading center. This implies that hydrothermal venting must be more widespread than previously assumed. In the case of Lost City, venting is the consequence of serpentinization reactions between seawater and fresh peridotite, which lead to formation of heat, hydrogen, and methane (3, 4). Typical for exothermic subsurface reactions with iron-bearing olivine, the hydrothermal fluids of Lost City are characterized by temperatures of 40° to 90°C, high pH (9 to 11), a low concentration of magnesium, and elevated concentrations of hydrogen and methane (1). Früh-Green et al. (5) found that this type of hydrothermal venting may have been present for more than 30,000 years at the Lost City field. This lifetime exceeds that of most of the known black smoker-type hydrothermal vents by at least two orders of magnitude. Considering Lost City's longevity and the active proliferation of methane and hydrogen, it seems odd that not much life was observed at this type of vent system, except for some cryptic microbial mats hidden inside the carbonate towers (1, 7).

Kelley and her collaborators went back to Lost City in 2003 for a month-long field expedition (2). With the research vessel Atlantis, the submersible Alvin, and the Autonomous Benthic Explorer (ABE) at their disposal, they were able to conduct detailed mapping of the vent field. This multidisciplinary research adventure is beautifully illustrated at http://www.lostcity.washington.edu/. A principal goal of the expedition was to discern how vent fluids, mineral precipitation, and microbial metabolisms interact to produce this extraordinary hydrothermal ecosystem and its underlying flow of energy and carbon.

The vent fluids of the Lost City system are very different from those of black smokers, white smokers, and other Mid-Atlantic Ridge systems fueled by serpentinization reactions. Seawater-basalt reactions driving volcanically hosted vents produce substantial amounts of CO2, sulfide in the millimolar range, and low pH (3 to 5), as well as extremely high temperatures (200° to 400°C). In contrast, the Lost City vents lack CO2 but provide high fluxes of hydrogen and methane at warm temperatures and high pH (see the figure, A). The fluids of other very iron- and magnesium-rich (ultramafic) vent systems at the Mid-Atlantic Ridge, such as at Logatchev and Rainbow, also show substantial methane and hydrogen anomalies but are distinguished by their much higher temperatures, low sulfide flux, and acidic pH (6). This difference between Lost City and other vent sites explains the lack of chemoautotrophic symbiotic organisms in Lost City fauna. Most of the reduced energy at the Lost City field is provided by hydrogen. Today, no animals are known to harbor hydrogen oxidizers as symbionts. Kelley et al. (2) found a high diversity of small invertebrates associated with the active carbonate structures, with a relatively high endemicity of nearly 60%. These invertebrates—snails, bivalves, polychaetes, amphipods, and ostracods—most likely derive some fraction of their energy requirement and carbon source by grazing on vent-associated carbonates and microbial biofilms (1).

A beehive of activity.

Microbial niches in serpentinization-influenced environments at the Lost City hydrothermal field. (A) Exothermic serpentinization reactions within the subsurface produce fluids of high pH enriched in methane and hydrogen, as well as some hydrocarbons. (B) Environments within the warm interior of carbonate chimneys in contact with end-member hydrothermal fluids host biofilms of Methanosarcina-like archaea (green circles). These organisms may play a dominant role in methane production and methane oxidation within the diverse environments present in the chimneys. Bacterial communities within these biotopes are related to the Firmicutes (purple rodlike cells). These organisms may be important for sulfate reduction at high temperature and high pH. (C) Moderate-temperature (40° to 70°C) endolithic environments with areas of sustained mixing of hydrothermal fluids and seawater support a diverse microbial community containing Methanosarcina-like archaea, ANME-1 (a methane-oxidizing phylotype; blue rectangular cells), and bacteria that include ϵ- and γ-proteobacteria (yellow filaments and red circles). The oxidation and reduction of sulfur compounds, the consumption and production of methane, and the oxidation of hydrogen most likely dictate the biogeochemistry of these environments. (D) In cooler environments (<40°C) associated with carbonate-filled fractures in serpentinized basement rocks, ANME-1 is the predominant archaeal phylotype. The bacterial populations contain aerobic methanotrophs and sulfur-oxidizing phylotypes.

CREDIT: TAINA LITWAK

The carbonate vents hold the key for understanding what is new about the metabolism, diversity, and distribution of microbial life at Lost City. An astonishingly high cell biomass is found inside the cavities and channel systems of the actively venting chimneys. The first analysis of such fluid-filled carbonate channels revealed the presence of archaeal biofilms (7). With their systematic study of diverse carbonate samples, Kelley et al. (2) now show that an almost pure culture of a new type of archaea develops in a specific setting within the chimneys characterized by direct contact with the hot end-member fluids (see the figure, B). The dominant archaea are phylogenetically related to the methanogenic archaea of the order Methanosarcinales. Interestingly, their closest relatives belong to ANME-3, a group of uncultivated anaerobic methanotrophs from cold-seep environments (8, 9). However, lipid biomarker analyses of the Lost City archaeal biofilms show an isotopic enrichment in 13C relative to source methane, indicative of a dominance of methanogenic growth. But the cooler parts of the vented carbonates appear to represent a crossroads between methanogenic and methanotrophic microniches (see the figure, C). This is indicated by the presence of both Methanosarcinales and ANME-1, as well as of functional genes indicative of anaerobic oxidation of methane (10, 11). The anaerobic oxidation of methane is assumed to function as a reversal of methanogenesis. However, no microorganism capable of switching between the two types of metabolism has yet been identified. Perhaps such an organism lives in Lost City. Indeed, physiological experiments with the new group of archaea dominating the Lost City vents may shed light on this question. Within carbonates hosted by basement rocks at ambient temperature (see the figure, D), gene and biomarker lipid analyses point to the coexistence of ANME-1 and sulfate-reducing bacteria, as in other methanotrophic ANME-1/carbonate habitats (12). Hence, abiotic and microbial methane production based on serpentinization reactions may be globally very high, but this methane appears to be directly consumed within neighboring microniches.

Ultramafic rocks favoring serpentinization reactions may have been some of the oldest habitats for microbial life on Earth. With their detailed study of the Lost City vent field, Kelley et al. present the first systematic portrayal of this type of subsurface ecosystem, which may still be widespread today. As proposed for early life on Earth and for potential life in outer space, this is an ecosystem in which abiotic methane and hydrogen production is exploited for anaerobic microbial methane and CO2 fixation as the primary processes for generating biomass. Intriguingly, the resulting biomass of the modern day analog at Lost City has an average isotopic carbon signature that we would not interpret as a signature of life, because it is not different from abiotic carbon sources. Hence, the submarine Lost City hydrothermal field discovered by Kelley and her team is one of the most interesting natural laboratories available to geologists, chemists and biologists, for studying the biogeochemical signatures of ecosystems driven by abiotic methane and hydrogen.

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