RESEARCH ARTICLE Fe [inferred to be Fe(II)] consistently exhibit
Distributions of concentration maxima deep in the drilled sed-
iment columns (e.g., Fig. 1). These con-
centration profiles indicate that biologically
Microbial Activities in Deep catalyzed reactions consume and release me-
tabolites deep in the sediment column at all
Subseafloor Sediments of the sites. The microbial processes implicit
in Fig. 1 include organic carbon oxidation,
Steven D’Hondt,1* Bo Barker Jørgensen,1 D. Jay Miller,1 ammonification, methanogenesis, methanotro-
Anja Batzke,2 Ruth Blake,1 Barry A. Cragg,1 Heribert Cypionka,1 phy, sulfate reduction, and manganese re-
Gerald R. Dickens,1 Timothy Ferdelman,1 Kai-Uwe Hinrichs,1 duction. Other processes that occur in these
sediments include iron reduction and the pro-
Nils G. Holm,1 Richard Mitterer,1 Arthur Spivack,1 Guizhi Wang,3
duction and consumption of formate, acetate,
Barbara Bekins,1 Bert Engelen,2 Kathryn Ford,1 Glen Gettemy,1 lactate, hydrogen, ethane, and propane (6).
Scott D. Rutherford,4 Henrik Sass,2 C. Gregory Skilbeck,1 These activities are unexpectedly diverse.
Ivano W. Aiello,1 Gilles Guerin,1 Christopher H. House,1
` The interstitial water chemistry of shallow
Fumio Inagaki,1 Patrick Meister,1 Thomas Naehr,1 marine sediments generally exhibits a pre-
Sachiko Niitsuma,1 R. John Parkes,1 Axel Schippers,1 dictable zonation, with peak concentrations
David C. Smith,1 Andreas Teske,1 Juergen Wiegel,1 of dissolved products from different redox
processes [Mn(II), Fe(II), SH2S, and CH4]
Christian Naranjo Padilla,1 Juana Luz Solis Acosta1
present at successively greater sediment
Diverse microbial communities and numerous energy-yielding activities depths (9–12). This succession of redox zones
occur in deeply buried sediments of the eastern Pacific Ocean. Distributions has been ascribed to competition between meta-
of metabolic activities often deviate from the standard model. Rates of bolic pathways; electron-accepting reactions
activities, cell concentrations, and populations of cultured bacteria vary that yield successively less negative standard
consistently from one subseafloor environment to another. Net rates of free energies are hypothesized to predomi-
major activities principally rely on electron acceptors and electron donors nate at successively greater depths because
from the photosynthetic surface world. At open-ocean sites, nitrate and electron acceptors with higher free energy
oxygen are supplied to the deepest sedimentary communities through the yields are depleted at shallower depths [e.g.,
underlying basaltic aquifer. In turn, these sedimentary communities may (9, 11)]. In shallow marine sediments that
supply dissolved electron donors and nutrients to the underlying crustal exhibit this zonation, terminal electron ac-
biosphere. ceptors ultimately enter the sediment from
the overlying ocean. As the reduced prod-
ucts from below enter successively shallower
Microbial life is widespread in the marine er are largely unknown. Its relationship to zones of SO42–, Fe(III), Mn(IV), NO3–, and
sediments that cover more than two-thirds of the photosynthetic surface world is not fully O2 reduction, vertical cascades of electron-
Earth_s surface. Intact cells (1) and intact understood. Its relationship to the deeper world accepting processes are sustained (11). For
membrane lipids (2, 3) provide evidence of of the underlying basaltic crust has not been example, O2 may be used to oxidize Mn(II)
prokaryotic populations in sediments as deep tested. to Mn(IV), which can oxidize Fe(II) to Fe(III),
as 800 m below the seafloor (mbsf). Prokaryotic To explore life in deeply buried marine which might oxidize reduced sulfur, which
activity, in the form of sulfate (SO42–) re- sediments, we undertook Ocean Drilling Pro- ultimately could oxidize hydrogen or organic
duction and/or methanogenesis, occurs in gram (ODP) Leg 201. The expedition sites carbon.
sediments throughout the world ocean (4). are located in the equatorial Pacific Ocean In many respects, dissolved chemical pro-
The prokaryotes of subseafloor sediments and on the continental margin of Peru (Fig. 1) files of Leg 201 sites exhibit this standard
have been estimated to constitute as much as (6). These sites are typical of subsurface en- zonation. However, they also depart from it
one-third of Earth_s total living biomass (5). vironments that exist throughout most of in four important ways. First, at site 1229,
Despite the ubiquity of life in subseafloor Earth_s ocean. Their water depths range from the introduction of dissolved SO42– from be-
sediments, little is known about it. The di- 150 m on the Peru Shelf to 5300 m in the low reverses the standard redox zonation by
versity of its metabolic activities, the com- Peru Trench. The sampled sediments ranged sustaining a zone with abundant SO42–
position of its communities, and the nature of in subseafloor depth from 0 to 420 m, in tem- beneath a sulfate-depleted methane-rich zone
its variation from one environment to anoth- perature from 1- to 25-C, and in age from 0 (Fig. 2). At this site and at nearby site 1228,
to 35 million years ago (Ma) (6, 7). Pro- SO42– is introduced at depth by upward dif-
Ocean Drilling Program Leg 201 Shipboard Scien- karyotic cells occur throughout the sampled fusion from ancient brine (6). This deep brine
tific Party. 2Institut fur Chemie und Biologie des
Meeres, Universitat Oldenburg, D-26111 Oldenburg, sediment column at every site (Fig. 1) (8). is present along much of the Peru Shelf (13).
Germany. 3University of Rhode Island Graduate Diversity of metabolic activities. Dis- At sites 1225 and 1226, SO42– similarly dif-
School of Oceanography, Narragansett, RI 02882, solved electron acceptors such as SO42– and fuses upward into the deepest sediments from
USA. 4Department of Environmental Science, Roger nitrate (NO3–) exhibit subsurface depletion, water circulating through the underlying ba-
Williams University, Bristol, RI 02809, USA.
whereas dissolved metabolic products such saltic aquifer. Sulfate is supplied to the deep-
*To whom correspondence should be addressed at as dissolved inorganic carbon (DIC 0 CO2 þ est sediments in this manner throughout much
NASA Astrobiology Institute, University of Rhode
Island Graduate School of Oceanography, South Ferry
HCO3– þ CO32–), ammonia (SNH3 0 NH3 þ of the eastern equatorial Pacific (14).
Road, Narragansett, RI 02882, USA. E-mail: dhondt@ NH4þ), sulfide (SH2S 0 H2S þ HS–), methane Second, at some sites, the expected zona-
gso.uri.edu (CH4), manganese [inferred to be Mn(II)], and tion is locally reversed by the appearance of
2216 24 DECEMBER 2004 VOL 306 SCIENCE www.sciencemag.org
large peaks in dissolved Mn and Fe concen- Third, subsurface CH4 maxima occur genesis occurs long before electron acceptors
trations far below the seafloor (e.g., Figs. 1 within the sediments of all Leg 201 sites, in- that yield higher standard free energies have
to 3). Such midcolumn peaks demonstrate cluding the open-ocean sites where dissolved been depleted.
that, in discrete intervals, concentrations of SO42– concentrations are high (6) (Fig. 1). The fourth important departure occurs
buried iron- and manganese-bearing minerals Similar maxima have recently been identi- only at the open-ocean sites, where the suc-
can be high enough and their rates of dis- fied at many other open-ocean sites (4, 15). cession of redox zones that extends from the
solution and reduction slow enough to con- They indicate that methanogenesis occurs seafloor to greater depths is mirrored by a
tinue long after metabolic activities with lower deep beneath the seafloor in most, perhaps similar succession that extends upward from
standard free energies have become predom- all, marine sediments, regardless of SO42– the basement-sediment interface (Fig. 3). At
inant in shallower sediments. availability. This result indicates that methano- sites 1225 and 1231, relatively high concen-
Fig. 1. Map of Leg 201 sites and concentration profiles of several dissolved chemical species at five of the sites (17). At sites 1225, 1226, and 1231, the
deepest sample was taken just above the basaltic basement.
0 Fig. 2. Concentration
profiles of cells and
some dissolved chemi-
cals at site 1229 (17).
50 White bands mark
sition zones. Arrows
mark midcolumn peaks
100 in dissolved Mn con-
4 5 6 7 8 9 10 11 0 10 20 30 40 0 1000 2000 3000 0 2 4 6 8 10
Cell concentration (Log10 cells cm-3) SO CH ( M)
Dissolved Mn ( M)
www.sciencemag.org SCIENCE VOL 306 24 DECEMBER 2004 2217
trations of NO3– and traces of O2 were dis- sulfate reduction) is similarly consistent with net fluxes of SH2S out of those sediments,
covered at the base of the sediment column this hypothesis. and estimated Fe reduction rates within the
(16, 17). This NO3– and O2 presumably enters The occurrence of methanogenesis in sediments are much higher at the ocean-
the sediments from oxic water circulating sulfate-replete porewaters and the occur- margin sites than at the open-ocean sites. In
through the underlying basaltic basement. rences of Mn and Fe reduction in deep methano- contrast, estimated Mn reduction rates and net
A local peak in dissolved Mn occurs just genic zones and deep sulfate-reducing zones NO3– reduction rates in the subsurface sed-
above this deep nitrate-reducing zone at both require different explanation(s) than the iments (from 91.5 mbsf to the base of the
sites 1225 and 1231 (Fig. 3). A similar peak reversed redox zones. There are at least drilled sediments) are higher at the open-ocean
occurs in the basal sediments of site 1226. three possible explanations of these occur- sites than at the ocean-margin sites. These net
At all three sites, these Mn concentration rences: (i) The organisms that undertake these NO3– reduction rates entirely result from the
maxima are stratigraphically overlain by maxi- different processes may rely on noncompet- introduction of NO3– from the underlying ba-
ma in dissolved Fe concentrations. These Mn itive substrates (different electron donors) saltic aquifers.
and Fe maxima mark successive intervals of in deep marine sediments; (ii) organisms These rates of subseafloor activities vary
Mn and Fe reduction. that rely on electron-accepting pathways with predictably from open-ocean sites to ocean-
The deep occurrences of successive O2, higher standard free energies may have higher margin sites (Table 1). At each site, the pre-
NO3–, Mn, and Fe redox zones at open-ocean energy requirements than organisms that rely dominant energy-yielding pathways may be a
sites have three immediate implications. First, on pathways with lower standard free energy function of total electron-accepting activity.
the transport of O2 and NO3– through the yields; or (iii) the in situ free energies of these For example, if the electron donor is C(0) for
underlying basaltic aquifer sustains aerobic reactions may differ greatly from their stan- electron-accepting reactions, carbon oxidation
and nitrate-reducing prokaryotic communities dard free energies (for example, all of these by net SO42– reduction appears to greatly
in the deepest (11 to 35 Ma) sediments of reactions may yield similar free energies in outpace carbon oxidation by metal (Mn and
these sites, although anaerobic communities deep subseafloor sediments where they co- Fe) reduction at the high-activity ocean-margin
are active in the overlying sediment. Second, occur). Whichever explanation ultimately sites and the most active open-ocean site
this deep introduction of NO3– and O2 may applies, subseafloor occurrences of many (Table 1) (20). In contrast, at the open-ocean
cause Mn and Fe oxidation fronts and electron-accepting activities cannot be pre- site where net activities are lowest (site 1231),
thereby sustain continued Mn and Fe cycling dicted by simple extrapolation of the shallow SO42– reduction is not detectable and net res-
at the base of the sediment column. Third, marine redox zonation to sediments at piration in sediments deeper than 1.5 mbsf
respiration along the flow path through the greater depths. may principally rely on reduction of Mn(IV)
underlying basalts is insufficient to strip O2 Rates of electron-accepting activities. At and Fe(III).
and NO3– from the circulating water. Respi- steady state, fluxes of SO42– and NO3– into a Biogeochemical linkages to the surface
ration in these basaltic aquifers may be sediment column are respectively equal to world and to life in underlying aquifers. The
limited by electron donor availability (18). net reduction rates of SO42– and NO3– within activities in Table 1 ultimately rely on elec-
These discoveries indicate that the energy- that column. Also at steady state, the mini- tron acceptors from the photosynthetically
yielding activities of deep subseafloor sedi- mum rate of metal (Mn or Fe) reduction is oxidized surface world. O2, NO3–, and SO42–
mentary ecosystems are far more diverse equal to the flux of the dissolved metal from ultimately enter these sediments by diffus-
than can be predicted from the standard redox zones of net reduction (marked by local con- ing down past the seafloor and, at the open-
zonation of shallow marine sediments. Al- centration peaks) to zones of net precipita- ocean sites, by transport upward from seawater
though unexpected, the reversed redox succes- tion or oxidation (marked by concentration flowing through the underlying basalts. The
sions of the deepest open-ocean sediments are minima) (19). oxidized Mn and Fe were originally intro-
consistent with the hypothesis that electron- Biogeochemical flux models based on con- duced to the sediments by deposition of Mn
accepting pathways with successively lower centration data and sediment physical prop- and Fe at the seafloor.
standard free energies predominate at suc- erties were used to quantify rates of these The activities in Table 1 probably also
cessively greater distances from a source of electron-accepting activities at most Leg 201 principally rely on electron donors from the
oxic water. The reversed subseafloor succes- sites (Table 1) (17, 19). Net rates of SO42– re- photosynthetically oxidized surface world. The
sion of site 1229 (from methanogenesis to duction in subseafloor sediments (91.5 mbsf), ultimate electron donors for subsurface eco-
Fig. 3. Dissolved concentration 0
profiles of NO3– (red diamonds),
Mn (light blue squares), and Fe
(dark blue circles) at open-ocean
sites 1225 (A), 1226 (B), and 1231 100
(C). Arrows mark midcolumn peaks
in dissolved concentrations of Mn
and Fe at site 1226. At each site,
the deepest sample was taken just 200
above the basaltic basement.
0 40 80 120 160 0 40 80 120 160 0 40 80 120 160
Concentration (µM) Concentration (µM) Concentration (µM)
2218 24 DECEMBER 2004 VOL 306 SCIENCE www.sciencemag.org
systems have been hypothesized to include trations are highest at sites where concen- site 1231 (25), this isolate demonstrates that
buried organic matter from the surface world trations of metabolic products (SNH3, CH4, previously undiscovered prokaryotes exist in
(9, 10), reduced minerals [such as Fe(II)- DIC) and net rates of SO42– reduction and Fe deep subseafloor sediments of the open ocean.
bearing silicates] (21, 22), and thermogenic reduction are highest, and cell concentra- Although the cultured bacteria constitute
CH4 from deep within Earth (23). Comparison tions are lowest at sites where these rates and only a small fraction of the total cell count in
of our subseafloor carbon oxidation estimates metabolic product concentrations are lowest each sample (up to 0.1%), these results hint
to published estimates of organic burial rates (Fig. 1 and Table 1). The open-ocean sites of consistent patterns in the community com-
(24) suggests that buried organic carbon from contained some of the lowest average cell position of subsurface sediments. Some lin-
the overlying photosynthetic world is abun- concentrations ever observed in deep-sea sed- eages appear to be cosmopolitan members
dant enough to fuel most or all of the esti- iments, whereas sediments recovered from of subseafloor sedimentary communities. The
mated electron-accepting activities (Table 1). the Peru Shelf contained the highest concen- most commonly cultured taxa are Firmicutes
The role of reduced minerals cannot be trations ever observed beneath the seafloor that are most closely related to the spore-
directly assessed with our data. However, (Fig. 2). forming bacterium Bacillus firmus and a-
thermodynamic considerations preclude oxi- Cell concentration profiles are also close- Proteobacteria that are most closely related
dation of Fe(II) or Mn by Fe(III) or SO42–. ly related to dissolved reactant distributions to Rhizobium radiobacter. These taxa were
Consequently, reduced Fe and Mn are unlikely within individual sites. For example, at site often recovered from open-ocean sediments
to be important subseafloor electron donors 1229, high cell concentrations occur in sub- with abundant dissolved SO42– and little CH4
at any sites where SO42– or Fe(III) is the seafloor sulfate-methane transition zones (Table 2). They were also often recovered
principal electron acceptor. In the sediments (Fig. 2). Diffusion of the two reactants from ocean-margin sediments with abundant
of site 1231, where Mn(IV) appears to be the (SO42– and CH4) to these zones provides an CH4 and no dissolved SO42–. Close relatives
principal electron acceptor, Fe(II) may be an interface of high biochemical energy supply. of R. radiobacter have also been recently iso-
important electron donor. At one such zone (92 mbsf), this interface lated from Mediterranean subseafloor sedi-
Our data clearly indicate that activity in supports cell densities that are an order of mag- ments (26). Recent surveys of archaeal 16S
the sediments of our open-ocean sites is not nitude higher than at the seafloor (Fig. 2). genes in subseafloor sediments suggest that
fueled by thermogenic CH4 from deep within Bacteria were successfully cultured and some archaeal lineages [the Deep-Sea Archaeal
Earth. Maximum concentrations in the mid- isolated from multiple depths at every site Group and the Marine Benthic Group A] are
dle of each open-ocean sediment column and (Table 2) (17). These cultures indicate that similarly cosmopolitan members of subsea-
minimum concentrations near the sediment- living bacteria are present throughout the en- floor sedimentary communities (27).
basement interface (Fig. 1) indicate that bio- tire range of subseafloor depths sampled by Other lineages appear to be more selec-
genic CH4 and SNH3 are produced deep in Leg 201 (1 to 420 mbsf) (Table 2). As as- tive in their subseafloor environmental affini-
these sediments, and, at sites where chemical sessed from the 16S ribosomal RNA (rRNA) ties. For example, cultured g-Proteobacteria
transport is dominantly diffusive, actually mi- genes of 168 isolates, these bacteria belong were consistently found at ocean-margin sites
grate downward toward the underlying basalts. to at least six distinct lineages (Table 2) (17). (Table 2), where concentrations of organic mat-
In this manner, the deep sedimentary com- Most of these isolates are closely related to ter, cell concentrations, and net metabolic rates
munities may provide electron donors and known marine organisms. Others are more are high. However, they were rarely found at
biologically accessible nitrogen to commu- distant from known organisms. Most striking- open-ocean sites, where organic concentra-
nities in the underlying basaltic aquifers. ly, the 16S gene of one isolate from open- tions, cell counts, and net metabolic rates are
Environmental variation in cell abun- ocean site 1225 differs from the 16S gene of low. In contrast, Actinobacteria were most
dance and cultured isolates of subseafloor its nearest known relative (a member of the consistently found in sulfate-reducing sedi-
sedimentary communities. Cell concentra- Bacteroidetes) by 14% (Table 2). In combi- ments of the open-ocean sites (sites 1225,
tions vary with metabolic reaction rates and nation with the recent discovery of deeply 1226, and 1231) and ocean-margin site 1227.
metabolic product concentrations from site rooted but previously unknown archaeal 16S In short, subseafloor sedimentary com-
to site (Fig. 1). For example, cell concen- gene sequences in subseafloor sediments of munities contain some taxa that inhabit a
Table 1. Estimated reduction rates and carbon oxidation equivalents at ODP Leg 201 sites. BDL, below detection limit; ND, not determined.
SH2S flux Potential Potential Organic
C oxidation C oxidation
Water Net NO3 – Estimated Estimated Net SO42– out of C oxidation C oxidation carbon
– by estimated by estimated
Leg 201 depth reduction Mn reduction Fe reduction reduction sediment by net NO3 by net SO42– burial
–2 –2 –2 (mol cm –2 Mn(IV) Fe(III)
location (m below (mol cm (mol cm (mol cm column reduction reduction rate (24)
–1) –1) –1) –1) –2 reduction reduction
sea level) year year year year (mol cm (mol cm –2 (mol cm –2 (mol cm –2
(mol cm –2 (mol cm –2
year –1) year –1) year –1) year –1)
year–1) year –1)
Peru margin sites
Shelf site 427 BDL 2.2 Â 10 –11 1.0 Â 10–7* 0.9 Â 10 –6 –0.7 Â 10 –6 BDL 1.1 Â 10 –11 2.5 Â 10 –8 1.8 Â 10 –6 3.1 Â 10 –6
Slope site 5086 ND 1.4 Â 10 –10 2.5 Â 10 –7* 2.5 Â 10–6 –2.0 Â 10 –6 ND 0.7 Â 10–10 6.3 Â 10 –8 5.0 Â 10 –6 3.1 Â 10 –6
Open Pacific sites
Equatorial 3760 1.3 Â 10 –9 2.9 Â 10–8 1 Â 10 –8* 1.9 Â 10 –8 BDL 1.6 Â 10 –9 1.5 Â 10 –8 2.5 Â 10 –9 3.8 Â 10 –8 4.5 Â 10 –7
Equatorial 3297 ND 5.9 Â 10 –9 7 Â 10 –8* 1.4 Â 10–7 –1.3 Â 10 –9 ND 3.0 Â 10 –9 1.8 Â 10 –8 2.8 Â 10 –7 4.6 Â 10–7
Peru Basin 4813 8.0 Â 10 –9 6.1 Â 10 –8 3.9 Â 10 –8 BDL BDL 1.0 Â 10 –8 3.0 Â 10 –8 1.0 Â 10 –8 BDL 9.4 Â 10 –7
*Inferred from net S burial. Assumes all buried S goes to FeS2.
www.sciencemag.org SCIENCE VOL 306 24 DECEMBER 2004 2219
Table 2. Cultured bacterial isolates from Leg 201 sediments. Species listed are type species from GenBank database.
Numbers of isolates (lowest and highest depth of discovery)
(16S rRNA Open Pacific sites Peru margin sites
1231 1225 1226 1227 1228 1229 1230
Rhizobium 7 (1 to 198 mbsf) 2 (1 to 381 mbsf) 14 (12 to 102 mbsf) 5 (12 to 70 mbsf) 13 (1 to 124 mbsf)
Rhodobacter 1 (268 mbsf)
Rhodovulum 1 (43 mbsf)
Bacillus firmus (97%) 14 (2 to 43 mbsf) 12 (1 to 420 mbsf) 8 (1 to 102 mbsf) 34 (1 to 187 mbsf)
Bacillus simplex (96%)* 1 (1 mbsf) 1 (70 mbsf)
Alkaliphilus 4 (1 mbsf)
Paenibacillus 1 (198 mbsf)
Vibrio 1 (101 mbsf) 6 (1 to 114 mbsf) 11 (1 to 187 mbsf)
Vibrio 1 (114 mbsf) 4 (1 to 82 mbsf)
Photobacterium 1 (1 mbsf)
Psychrobacter 3 (1 to 124 mbsf)
Marinobacter 1 (268 mbsf)
Marinobacter 2 (268 mbsf)
Micrococcus 2 (1 to 307 mbsf) 1 (381 mbsf)
Kocuria palustris (99%) 4 (21 to 40 mbsf)
Oerskovia 3 (2 to 101 mbsf) 5 (40 to 55 mbsf)
Desulfomicrobium 2 (103 mbsf)
Porphyromonas 1 (198 mbsf)
*Species names identify the type species in the GenBank database that are the closest relatives of the cultured isolates. The genetic distance between each cultured taxon and its
closest relative is illustrated by the percent similarity of their 16S rRNA sequences.
broad array of redox environments and other effects on mineral, chemical, and biological to be late Eocene on the basis of planktic microfossil
taxa that appear to exhibit consistent prefer- resources are poorly constrained. The mini- 8. Leg 201 microbiological studies relied on samples
ences for specific subseafloor environments. mum energy fluxes required to sustain them that had very low or undetectable contamination, as
At least some of the former taxa are cos- remain unknown. Their total genetic diver- assessed by our contaminant tracing tests (17).
mopolitan in their distribution. This broad sity, rates of population turnover, detailed 9. P. N. Froelich et al., Geochim. Cosmochim. Acta 43,
distribution is not entirely surprising, given metabolic interactions, and community struc- 10. K. H. Nealson, Annu. Rev. Earth Planet. Sci. 25, 403
(i) the occurrence of so many of the same tures remain to be determined. (1997).
metabolic products and reactants at every 11. B. B. Jørgensen, in Marine Geochemistry, H. D. Schulz,
References and Notes M. Zabel, Eds. (Springer-Verlag, Berlin, 2000), pp.
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1. R. J. Parkes, B. A. Cragg, P. Wellsbury, Hydrogeol. Rev.
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Org. Geochem. 34, 755 (2003). 85–128.
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2067 (2002). (2002).
which organisms (cultured or uncultured) are 5. W. B. Whitman, D. C. Coleman, W. J. Wiebe, Proc. 16. Traces of dissolved O2 were detected at the top and
responsible for which metabolic activities in Natl. Acad. Sci. U.S.A. 95, 6578 (1998). bottom of the site 1225 and site 1231 sediment
these sediments. We have probably not yet 6. S. D’Hondt et al., Proc. ODP Init. Rep. 201 [CD-ROM] columns (6). These data were too few and too
(2003). imprecise to use for estimating O2 fluxes (17).
reached the greatest sedimentary depths that
7. The youngest sediments are from the seafloor. The 17. See supporting data on Science Online.
subseafloor organisms attain. Their effects oldest sediment is from the base of the sediment 18. From alteration textures and chemical traces, pro-
on global biogeochemical cycles and their column at Peru Basin site 1231; its age is estimated karyotic life has been inferred to occur in the glassy
2220 24 DECEMBER 2004 VOL 306 SCIENCE www.sciencemag.org
rinds of oceanic basalts (21). Fe and S in sub- with depth (1), more than 99% of the total biomass 27. A. Lauer, A. Teske, Int. J. Astrobiol. 3 (S1), 63 (2004).
seafloor basalts are strongly oxidized in the first in sediments deeper than 1.5 mbsf lies within our 28. Samples, shipboard facilities, and expedition support
10 million to 20 million years of the basalts’ ex- calculational interval at each site. were provided by the ODP. The NASA Astrobiology
istence (22). Oxidation of these chemical species 20. Two moles of C(0) (organic carbon) are oxidized by Institute (NAI) supported postcruise analysis of
has the potential to support abundant biomass in reducing one mole of SO4 2– to S2–. Five moles of biogeochemical data and precruise development of
basaltic aquifers (22, 23). Our results indicate that C(0) are oxidized by reducing four moles of NO3 – shipboard biogeochemical techniques. Postcruise
by 11 Ma and 35 Ma at sites 1225 and 1231, re- to two moles of N2. Four moles of Fe(III), or two culturing studies were supported by grants from the
spectively, such oxidation is insufficient to strip moles of Mn(IV), are required to oxidize one mole Deutsche Forschungsgemeinschaft. We thank three
dissolved O2 and NO3 – from the circulating water, of C(0). anonymous reviewers for very helpful comments.
perhaps because the mineral surfaces in contact 21. M. R. Fisk, S. J. Giovannoni, I. H. Thorseth, Science
with water were largely oxidized when the basalt 281, 978 (1998). Supporting Online Material
was younger. 22. W. Bach, K. J. Edwards, Geochim. Cosmochim. Acta www.sciencemag.org/cgi/content/full/306/5705/2216/
19. At each site, the sediment column for which fluxes 67, 3871 (2003). DC1
were calculated spans the interval from 1.5 mbsf to a 23. T. Gold, Proc. Natl. Acad. Sci. U.S.A. 89, 6045 (1992). Materials and Methods
point midway between the two deepest sample 24. R. A. Jahnke, Global Biogeochem. Cycles 10, 71 (1996). References
depths. At the open-ocean sites, this interval ends 25. K. B. Sørensen, A. Lauer, A. Teske, Geobiology, in press.
just above the sediment-basalt contact. Given an 26. ¨
J. Suß, B. Engelen, H. Cypionka, H. Sass, FEMS 7 June 2004; accepted 15 October 2004
exponential decline in average cell concentrations Microbiol. Ecol., in press. 10.1126/science.1101155
Recently, it has been shown in an x-ray
Electron Coherence in a Melting diffraction experiment that this limitation can
be overcome by working on the interface of a
Lead Monolayer liquid and a crystalline material, which led to
the first experimental observation of the five-
F. Baumberger,* W. Auwarter,. T. Greber, J. Osterwalder-
¨ fold local symmetry (9), predicted for mon-
atomic 3D liquids more than 50 years ago
We used angle-resolved photoemission spectroscopy to measure the elec- (10). We use a similar idea to directly mea-
tronic dispersion and single-particle spectral function in a liquid metal. A lead sure the electron dispersion and spectral func-
monolayer supported on a copper (111) surface was investigated as the tem- tion in a 2D liquid: melted Pb. A crystalline
perature was raised through the melting transition of the film. Electron spec- Cu(111) substrate serves as a support with
tra and momentum distribution maps of the liquid film revealed three key minimal influence on the atomic arrange-
features of the electronic structure of liquids: the persistence of a Fermi sur- ment of the 2D Pb liquid, and at the same
face, the filling of band gaps, and the localization of the wave functions upon time ensures that the parallel momentum of
melting. Distinct coherence lengths for different sheets of the Fermi surface the initial Pb states is conserved in the
were found, indicating a strong dependence of the localization lengths on the photoemission process. In a crystalline envi-
character of the constituent atomic wave functions. ronment, the momentum needed for photo-
emission is supplied in discrete quantities by
The transition from the solid to the liquid tal). In random systems, such as amorphous reciprocal lattice vectors, whereas in a liquid,
state can have substantial effects on a mate- solids or liquids, the crystal momentum is no the photoelectrons gather arbitrary momenta
rial_s electronic properties (1, 2). In the case longer a good quantum number and the prob- in the process. For a liquid monolayer, how-
of semiconducting germanium, for example, lem becomes analytically intractable (1, 5, 6). ever, the momentum of the initial state can
the forbidden states in the band gap of the Despite decades of intense research, be retrieved, because the proximity of the
crystal are filled and the melt is metallic many fundamental problems of the electron- crystalline substrate allows transfer of re-
(3, 4). Understanding the evolution of the ic structure of liquids remain unresolved (7). ciprocal lattice vectors to the liquid states.
electronic wave functions, which underlie such In particular, the character of the electronic Complete momentum distribution maps of
marked changes of the physical properties, wave functions (e.g., to what extent they are the liquid film indicate two Fermi surface
represents a prime experimental and theoret- itinerant or localized) has eluded experimen- sheets, and the spectral function (measured
ical challenge. The main conceptual issue is tal investigation. The primary experimental independently for both sheets) reveals novel
the lack of any long-range order in liquid or problem is the loss of periodicity, which re- aspects of the electronic structure of liquids.
amorphous materials. The periodicity of crys- stricts the information provided by the most Contrary to the usual assumptions that ac-
talline solids allows the classification of elec- important experimental probes. A diffraction company the concept of a mobility edge, we
tronic wave functions as Bloch states (i.e., experiment, which can retrieve the full three- find only a negligible energy dependence of
plane waves, modulated by lattice periodic dimensional (3D) atomic structure of a the localization length (spatial extension of an
functions, that extend through the entire crys- crystalline material, yields only a 1D projec- exponentially decaying wave function) but a
tion in the form of a pair-correlation length marked momentum dependence. This is in-
Physikinstitut der Universitat Zurich, Winterthurer-
¨ in a liquid or amorphous material (8). Analo- terpreted as a manifestation of the different
strasse 190, CH-8057 Zurich, Switzerland.
¨ gously, angle-resolved photoemission spectros- symmetries of the constituent atomic orbitals.
*Present address: Department of Applied Physics, copy (ARPES), which gives direct access to The experiments were performed in a mod-
Stanford University, Stanford, CA 94305, USA. the single-particle spectral function A(k,w) ified VG-ESCALAB 220 spectrometer (11)
.Present address: Department of Physics and Astron- in crystals, only measures the projection of using He Ia radiation (21.22 eV). The energy
omy, University of British Columbia, Vancouver,
British Columbia V6T1Z4, Canada.
the momentum-resolved quantity on the en- and angular resolutions were set to 60 meV
-To whom correspondence should be addressed. ergy coordinate (i.e., the spectral density) in and T0.4-, respectively. Pb was evaporated
E-mail: email@example.com a liquid. resistively onto a clean Cu(111) surface held
www.sciencemag.org SCIENCE VOL 306 24 DECEMBER 2004 2221