The Subseafloor Biosphere at Mid-Ocean Ridges

391 Pages·47.899 MB·English

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Geophysical Monograph 144
The Subseafloor Biosphere
at Mid-Ocean Ridges
William S.D. Wilcock
Edward F. DeLong
Deborah S. Kelley
John A. Baross
S. Craig Cary
Editors
88 American Geophysical Union
Washington, DC 2004
Published under the aegis of the AGU Books Board
Jean-Louis Bougeret, Chair, Gray E. Bebout, Cari T. Friedrichs, James L. Horwitz, Lisa A. Levin, W. Berry Lyons,
Kenneth R. Minschwaner, Andy Nyblade, Darrell Strobel, and William R. Young, members.
Library of Congress Cataloging-in-Publication Data
The subseafloor biosphere at mid-ocean ridges / William S.D. Wilcock ... [et al.], editors,
p. cm — (Geophysical Monograph ; 144)
Includes bibliographical references.
ISBN 0-87590-409-2
1. Deep-sea ecology—Congresses. 2. Mid-ocean ridges—Congresses. I. Wilcock, Wiliam S.D., 1963-11. RIDGE
Theoretical Institute on the Subsurface Biosphere at
Mid-Ocean Ridges (5th : 2000 : Big Sky, Mont.) III. Series.
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577.7'9-dc222
2004043681
ISBN 0-87590-409-2
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Copyright 2004 by the American Geophysical Union
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Front Cover: Shaded bathymetric relief map of the Earth's oceans color coded by the age of the basement with colors
ranging from red for young oceanic crust near ocean spreading centers to blue for the oldest crust (courtesy Center for
Environmental Visualization, University of Washington with bathymetric data from W. Smith and D. Sandwell and
digital isochrons from R. Muller, W. Roest, J.-Y. Royer, L. Gahagan and J. Sclater). The left portion of the top inset
image is the Strawberry Fields sulfide structure on the Endeavour segment of the Juan de Fuca Ridge with Ridgeia
piscesae tubeworms in the foreground (courtesy J. Delaney, D. Kelley and the Canadian Scientific Submersible Facility).
The right portion is a combination phase contrast/fluorescence micrograph of a 50-micron iron oxide aggregate with
attached hyperthermophilic archaeon GR1 (blue), which was isolated from an event plume associated with the 1996
North Gorda eruption on the Juan de Fuca Ridge (courtesy M. Holland). The bottom inset image shows a tubular pillow
basalt surrounded by Calyptogena vent clams from the Caly Field low-temperature hydrothermal site on the Galapagos
Rift at 89.5°W (courtesy D. Fornari, T. Shank, S. Hammond and R. Haymon and The Woods Hole Oceanographic
Institution - Deep Submergence Operations Group).
Back Cover: The left image shows a small collapse in lobate lava from the East Pacific Rise near 9° 50'N during a
seafloor eruption in 1991. The white coating on the lava is bacterial by-products generated by microbial activity asso­
ciated with the eruption (courtesy D. Fornari, T. Shank, S. Hammond and R. Haymon and The Woods Hole
Oceanographic Institution - Deep Submergence Operations Group). The right image shows tubular corrosion features
caused by microbially mediated dissolution of volcanic glass (courtesy H. Staudigel and H. Furnes).
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CONTENTS
Introduction
The Subsurface Biosphere at Mid-Ocean Ridges: Issues and Challenges
John A. Baross, William S. D. Wilcock, Deborah S. Kelley, Edward F. DeLong, 5. Craig Cary 1
Physical Limits to Subsurface Life
The Upper Temperature Limit for Life Based on Hyperthermophile Culture Experiments
and Field Observations
James F. Holden and Roy M. Daniel 13
The Stability of Biomolecules and the Implications for Life at High Temperatures
Roy M. Daniel, James F. Holden, Jolanda Truter, Don A. Cowan, and Renate van Eckert 25
On the Edge of a Deep Biosphere: Real Animals in Extreme Environments
James J. Childress, Charles R. Fisher, Horst Felbeck, and Peter Girguis 41
The Subseafloor Environment at Mid-Ocean Ridges
Geophysical Constraints on the Subseafloor Environment Near Mid-Ocean Ridges
William 5. D. Wilcock and Andrew T. Fisher 51
Diking, Event Plumes, and the Subsurface Biosphere at Mid-Ocean Ridge
Robert W. Embley and John E. Lupton 75
Fluid Flow and Fluid-Rock Interaction Within Ocean Crust: Reconciling Geochemical,
Geological, and Geophysical Observations
Wolfgang Bach, Susan E. Humphris, and Andrew T. Fisher 99
Serpentinization of Oceanic Peridotites: Implications for Geochemical Cycles
and Biological Activity
Gretchen L Fruh-Green, James A. D. Connolly Alessio Plas, Deborah S. Kelley,
and Bernard Grobety 119
Environmental Conditions Within Active Seafloor Vent Structures: Sensitivity to Vent Fluid
Composition and Fluid Flow
Margaret Kingston Tivey 137
Energy Sources and Physiological Diversity
Geochemical Energy Sources That Support the Subsurface Biosphere
Everett L. Shock and Melanie E. Holland 153
Volatiles in Submarine Environments: Food for Life
Deborah S. Kelley Marvin D. Li I ley, and Gretchen L. Fruh-Green 167
Activation of Diatomic and Triatomic Molecules for the Synthesis of Organic Compounds:
Metal Catalysis at the Subseafloor Biosphere
George W. Luther, III 191
Potential Importance of Dissimilatory Fe(lll)-Reducing Microorganisms
in Hot Sedimentary Environments
Kazem Kashefi, Dawn. E. Holmes, Derek R. Lovley, and Jason M. Tor 199
Significance of Polysaccharides in Microbial Physiology and the Ecology of
Hydrothermal Vent Environments
Marybeth A. Pysz, Clemente I. Montero, Swapnil R. Chhabra, Robert M. Kelly and
Kristina D. Rinker 213
Environmental Dynamics and Variability
Detection of and Response to Mid-Ocean Ridge Magmatic Events: Implications for
the Subsurface Biosphere
James P. Cowen, Edward T. Baker, and Robert W. Embley 227
Diffuse Flow Hydrothermal Fluids From 9°50'N East Pacific Rise: Origin, Evolution and
Biogeochemical Controls
Karen L. Von Damm and Marvin D. Lilley 245
Mixing, Reaction and Microbial Activity in the Sub-seafloor Revealed by
Temporal and Spatial Variation in Diffuse Flow Vents at Axial Volcano
David A. Butterfield, Kevin K. Roe, Marvin D. Lilley Julie A. Huber, John A. Baross,
Robert W. Embley and Gary J. Massoth 269
Illuminating Subseafloor Ecosystems Using Microbial Tracers
Melanie E. Holland, John A. Baross, and James F. Holden 291
Sedimented Ridges as a Laboratory for Exploring the Subsurface Biosphere
Robert A. Zierenberg and Melanie E. Holland 305
Global Distribution and Comparisons
The Ocean Crust as a Bioreactor
Hubert Staudigel, Bradley Tebo, Art Yayanos, Harald Furnes, Katie Kelley,
Terry Plank, and Karlis Muehlenbachs 325
Diversity of Life at the Geothermal Subsurface-Surface Interface:
The Yellowstone Example
John. R. Spear and Norman R. Pace 343
Unifying Principles of the Deep Terrestrial and Deep Marine Biospheres
Frederick S. Colwell and Richard P. Smith 355
Distribution of Unusual Archaea in Subsurface Biosphere
Ken Takai, Fumio Inagaki, and Koki Horikoshi 369
Future Directions
Studying the Deep Subsurface Biosphere: Emerging Technologies and Applications
S. Craig Cary, Barbara J. Campbell, and Edward F DeLong 383
PREFACE
Awareness has grown over the past several years that the includes papers that review previous work in light of the
subseafloor may harbor a substantial biosphere sustained by recent upsurge of interest in the subseafloor biosphere and
volcanic heat and chemical fluxes from the Earth's interior. original research with new insights. As a whole, the mono­
This realization has profound scientific implications for graph provides a comprehensive synthesis of our current
questions concerning the origins of life, the true extent of state of knowledge while discussing key questions and
Earth's biosphere, and the search for life on other planets. At approaches that will motivate future work.
mid-ocean spreading centers, the fluxes that sustain life are The volume opens with an introductory overview of key
the highest, and the hydrothermal fluids in which micro­ questions that stimulate us to study the subseafloor bio­
organisms grow are readily accessible on the seafloor. In sphere near mid-ocean ridges. All but the final articles are
addition, periodic volcanic eruptions flush fluids and grouped into five sections, each of which presents a different
microbes from the subsurface, and volcanic gases are approach. Because the subseafloor is an extreme environ­
believed to drive spectacular microbial blooms. Although ment, the first section examines the physical limits of life.
ridges are challenging locations in which to work, they are The second section examines the geological constraints on
unique in the oceans because of the diversity and dynamic crustal structure and processes with a particular emphasis on
nature of their subsurface environments. hydrothermal flow. As life depends on the availability of
Subsurface geological and biological processes are inextri­ suitable energy sources, the third section examines the avail­
cably linked at ridges. Not only do volcanoes provide the ability of chemical energy and nutrients in the subsurface
habitat, energy, and nutrients to support life, but also physi­ subseafloor and some implications for physiological diver­
cal and chemical processes within young crust provide fun­ sity. The fourth section describes the results of several field
damental controls on the ecology and perhaps the diversity of studies designed to understand the subseafloor biosphere,
microbial communities. Biological feedback may signifi­ which illustrate the challenges and potential of working in
cantly influence hydrothermal fluids and crustal aging as this dynamic environment. The final section sustains discus­
well. Recent advances in microbial analysis techniques and sion on the broader distribution of the subsurface biosphere
in our ability to operate and make long-term observations on and compares mid-ocean ridges to other subsurface environ­
the seafloor have advanced our understanding of mid-ocean ments. The volume concludes with a discussion on the impli­
ridge hydrothermal systems and organisms that thrive in this cations of new and emerging microbial techniques to future
environment. At the same time, because the subseafloor is studies of the subseafloor biosphere.
difficult to sample directly and the system is so complex, we The monograph is an outgrowth of the Fifth RIDGE
still have much to learn. Indeed some of the most basic Theoretical Institute on "The Subsurface Biosphere at Mid-
characteristics of the subseafloor biosphere in young ocean Ocean Ridges," which was held in Big Sky, Montana, sum­
crust, such as its physical dimensions, biomass, and composi­ mer 2000. Most of the papers in this volume derive from pre­
tion, are poorly known and represent a key impetus for ongo­ sentations and discussions at that meeting. We thank Dave
ing and future studies. Christie, Carol Chin, and Chris LeBoeuf in the RIDGE
With such issues in mind, this monograph presents contri­ Office for their work promoting and organizing the meeting.
butions from marine geoscientists and biologists who have We also thank our colleagues who attended the meeting and
worked extensively on mid-ocean ridge systems as well as the reviewers of papers in this volume who provided a high
from an ever expanding community of microbiologists who, level of peer review. We acknowledge the assistance of our
while new to this environment, have already developed tech­ acquisitions editor, Allan Graubard, and the oversight of
niques and insights important to our work. The volume AGU's book production staff in seeing the book into print.
The Subsurface Biosphere at Mid-Ocean Ridges:
Issues and Challenges
John A. Baross, William S. D. Wilcock, and Deborah S. Kelley
School of Oceanography, University of Washington, Seattle
Edward F. DeLong
Monterey Bay Aquarium Research Institute, Moss Landing, California
S. Craig Cary
Center for Marine Genomics, University of Delaware, Lewes, Delaware
A recent growth of interest in subsurface microbiology has been fueled by the
recognition that the subsurface may have played an important role in the origin
and early evolution of life, and may presently sustain a substantial fraction of
Earth's biomass. The uppermost igneous oceanic crust is likely to be one of the
most habitable subsurface environments because it is porous and the locus of
extensive hydrothermal circulation. This circulation is most vigorous at spreading
centers where it is driven by the volcanic accretion of oceanic crust. Hot reduced
hydrothermal fluids created by water-rock reactions above magma bodies mix
with cold seawater in the subsurface and the resulting chemical disequilibria pro­
vide energy and carbon sources that support diverse microbial communities.
These communities can be sampled in chronic low-temperature hydrothermal
vents and in the hydrothermal fluids released following volcanic eruptions.
Investigations of the subseafloor environment at mid-ocean ridges integrate bio­
logical and geological approaches to understand the characteristics of hydrother­
mal circulation and how they are modulated by geological events; the sources of
carbon, nutrients and energy; and the types and functions of subsurface organisms.
They also utilize analogies with accessible sulfide edifices and comparisons with
similar subsurface environments elsewhere. Future studies will combine increasi­
ngly sophisticated shore-based studies with data from long-term observatories
comprising networks of instruments for measuring key physical, chemical and
microbial parameters. They will require the development of technology to drill
bare rock mid-ocean ridge sites, collect uncontaminated subsurface samples and
deploy instruments at different depths in the crust.
1. INTRODUCTION
The Subseafloor Biosphere at Mid-Ocean Ridges Oceanography has changed remarkably over the past
Geophysical Monograph Series 144 30 years. Historically, it was largely an expeditionary sci­
Copyright 2004 by the American Geophysical Union ence in which the research objectives were framed within
10.1029/144GM01 individual disciplines and limited by the paucity and short
duration of observations. Today, the field is benefiting from limits of life, broadened the possible habitable zones both
a rapid expansion of our capabilities to survey the oceans on Earth and elsewhere, and contributed to the development
and the seafloor, collect samples, and make long-term of the new field of astrobiology, which seeks to better
observations. At the same time, revolutionary developments understand how life has evolved on Earth and to use this
in fields such as molecular biology and the exponential knowledge to guide search strategies on other planetary
growth of computational power have introduced a new array bodies [Des Marais et ah, 2003].
of methods to analyze samples and model data at sea and The current level of interest in seafloor hydrothermal sys­
ashore. Oceanographic research is increasingly driven by tems is well illustrated by a number of other nearly concurrent
questions that are inherently multi-disciplinary and require volumes devoted to aspects of the field [Halbach et ah, 2003;
ambitious long-term observational programs. Davis and Elderfield, 2004; German et ah, 2004]. This vol­
Nowhere are these changes more apparent than in the field ume focuses on the subseafloor biosphere at mid-ocean ridges
of submarine hydrothermal vent research. Hydrothermal and in particular our present understanding of its dimensions
vents and their oases of bizarre animals nurtured by micro­ and inhabitants, the physical and chemical factors that control
organisms were first discovered a little over a quarter of its characteristics, the role microbes play in shaping this envi­
a century ago [Corliss et ah, 1979]. Their discovery con­ ronment and its relationship to the subsurface biosphere else­
firmed earlier inferences about the importance of hydrother­ where. It is the product of an NSF-funded RIDGE Theoretical
mal circulation for cooling the young oceanic lithosphere Institute on "The Subsurface Biosphere at Mid-Ocean
[Lister, 1972] and for facilitating chemical exchange Ridges" that was held in Big Sky, Montana in the summer of
between the oceanic crust and oceans [Craig et ah, 1975]. 2000. One of the clear messages to come from this meeting
Chemosynthetic life forms found at the vents provided a and which is a ongoing theme in this volume is that input from
new direction for biological research [Cavanaugh et ah, all of the disciplines currently involved in mid-ocean ridge
1981; Jannasch, 1984] and fostered speculation about the research will be required to understand the complex geo-
role of volcanoes in the origin and evolution of early life biological interactions operative in these dynamic systems.
[Corliss et ah, 1981]. However, the early field studies were Many of the papers are co-authored by scientists working in
primarily confined to visual observations and sampling dur­ different disciplines and they provide first-hand proof of the
ing infrequent visits and in most cases research proceeded importance of linking biology and geosciences to design
along separate geological and biological tracks. experiments that address key questions regarding the extent
Today the picture is quite different. Increasingly higher and significance of a subseafloor biosphere.
resolution maps of the seafloor and geophysical images of
the subsurface are integrated with more sophisticated tech­ 2. BACKGROUND
niques to obtain extensive rock and fluid samples.
Integrated data sets from these studies have been combined 2.1. Life in the Subsurface
with analyses of fossil hydrothermal systems in ophiolites
to gain a better appreciation of the structure of hydrother­ There are few published studies of life in the subsurface
mal systems and their role in the formation and alteration of prior to the 1960's and 1970's. Sulfate reducing bacteria
oceanic crust. Efforts to monitor mid-ocean ridges in real or were detected in oil well brines at depths greater than 300 m
near-real time have demonstrated that volcanic and tectonic [Bastin, 1926; Bastin and Greer, 1930] and in coal deposits
events have a profound effect on hydrothermal circulation to 1089 m [Lieske and Hoffmann, 1929]. Similarly, bacteria
and biological activity. Recent developments in biology and were detected in a 6 m sediment core [Emery and Dietz,
molecular biology have provided new tools for assessing 1941] and it was noted that the numbers of viable bacteria
the diversity of small organisms including bacteria and decreased with depth in sediment cores [ZoBell, 1942].
viruses that have resisted detection by conventional cultur- While these pioneering studies were interesting, the methods
ing and microscopic methods. As in most other environ­ available for estimating the incidence and diversity of
ments, microorganisms in seafloor hydrothermal systems microorganisms were limited and greatly underestimated the
have been found to be much more abundant and diverse biomass in these environments.
than initially inferred. Novel microorganisms have been More recently, subsurface microbiology has been the
discovered that grow in the subsurface under extreme ther­ focus of considerable research by diverse groups of scien­
mal and chemical conditions that were previously thought tists. This interest stems in part from the possibility that the
to be sterile. It has also become increasingly apparent that subsurface biomass may exceed that of the earth's entire sur­
many organisms may have a profound effect on subsurface face. Such was the message in Thomas Gold's seminal paper
geochemical cycles. These findings have significantly [Gold, 1992], which was based on calculations of pore space
altered our perception about the physical and chemical and temperatures permissible for life in the subsurface.
BAROSS ET AL. 3
A more recent estimate indicates that the subsurface repre­ axis passive hydrothermal circulation is driven by heat flow
sents 90-94% of all prokaryotic cells on Earth [Whitman from the cooling lithosphere and continues out to crustal ages
et al, 1998] and this proportion may grow as we learn more of at least 65 Myr, initially in systems that are open to the
about microbial communities in oceanic crust. Missing in seafloor and subsequently in closed systems that are sealed by
Gold's message were discussions of how liquid water could a cap of impermeable sediments [Stein and Stein, 1994].
circulate into the deep subsurface and the sources of carbon, Sampling subsurface sections of oceanic crust is difficult
nutrients and energy resources that could support a subsur­ and most samples for microbiological and chemical analyses
face biosphere. These are among the key issues that drive are from variable mixtures of seawater and hydrothermal
much present day research. fluids from axial upflow zones or from fluids escaping from
Over the past 20 years, microorganisms have been dis­ basement crust off axis at drill-hole sites and seamounts that
covered below the surface of the Earth's crust, in many penetrate through old sediment [Wheat et al, 2002]. These
environments once thought sterile including all sampled fluid samples have yielded important information about the
subsurface environments with liquid water. The environ­ phylogenetic and physiological diversity of the subseafloor
ments include oil wells, deep granitic and basaltic aquifers, microbial community and the chemical characteristics that
sandstone cores, clays, gold mines, hot gold seams, and control this diversity [Holden et al, 1998; Holland et al,
deep sediments [Boivin-Jahns et al, 1996; Balkwill this volume]. However, so far we have not been able to visu­
et al, 1997; Krumholz et al, 1997; Pedersen, 1997; Onstott alize the microbial communities in their specific biotopes
et al, 1999; Sievert and Kuever, 2000; Inagaki et al, 2003; within the crust, their spatial distribution and interaction
Roling et al, 2003; Colwell and Smith, this volume]. with minerals, their interaction as a community and how
Methanogens, sulfate and iron reducers, and acetogens are they exploit energy and nutrient resources.
commonly isolated from all these environments. Anaerobic
hyperthermophiles are also consistently found in oil wells 2.2. Life in Mid-Ocean Ridge Hydrothermal Systems
[Stetter et al, 1993; Grassia et al, 1996; Slobodkin et al,
1999; Orphan et al, 2000]. However, most deep terrestrial Ridge-crest hydrothermal systems are commonly divided
subsurface environments have very sparse populations of into three zones, the recharge, reaction, and upflow zones
slow growing microorganisms [Kerr, 2002]. [e.g., Lowell et al, 1995]. In the recharge zone, seawater
Because subseafloor basement is difficult to sample, most sinks into the crust over a poorly defined but potentially quite
of the microbiological research in the subseafloor has extensive region. Geochemical data shows that sea-water in
focused on deep sediments. Most of the data consists of the recharge zone can reach 150°C at the sheeted dike layer
microscopic counts of fluorescently stained microorganisms [Alt et al, 1986; Gillis and Robinson, 1990], an observation
and fatty acid analyses [Cragg and Parkes, 1994; Parkes indicating that much of the shallow recharge zone is at tem­
et al, 1994; Summit et al, 2000; Zierenberg and Holland, peratures that allow microbial growth. Although there are no
this volume]. Generally, the studies confirm the findings of direct observations of microbes in recharge zones for axial
ZoBell [1942] that the numbers of microorganisms decrease systems, some predictions can be made about the metabolic
significantly with depth and there are very low numbers of potential of these communities based on chemical measure­
microorganisms in deep sediment cores. There is only limi­ ments made off-axis. The recharge biosphere is likely sup­
ted information about deep sediment microorganisms; they ported by electron acceptors such as nitrate and sulfate and
inhabit separate zones of sulfate reduction and methanoge- possibly oxygen, and electron donors such as Fe (II) and sea­
nesis and have metabolic rates that are extremely slow water derived organic matter [Alt, 1995].
[D'Hondtet al, 2002]. The reaction zone is the region in the mid-crust where
Even less is known about microbial communities in downwelling fluids begin to react chemically with basaltic
igneous oceanic crust even though it is predicted that of all rock [e.g., Butterfield et al, 2003]. This zone encompasses
deep environments, it contains the most favorable habitat for a wide range of temperatures and redox conditions, but at
microbial life. The uppermost igneous crust, in particular, is 350-450°C important fluid-rock reactions occur that result
highly porous and permeable. At the ridge axis, vigorous cir­ in the leaching of volatiles and metals from the basaltic sub­
culation (commonly termed active circulation [Lister, 1982]) strates. This high-temperature zone represents the root of the
is driven by the magmatic heat that must be removed to solid­ hydrothermal system and is bounded by hot crystalline
ify and cool the oceanic crust. This circulation occurs in sin­ material that may or may not be associated with an active
gle-pass circulation cells that are open to the seafloor. The magma chamber that contains melt [Kelley et al, this vol­
high temperatures and fluid fluxes mediate extensive water- ume]. It is at the base of the system where fluids heat up
rock reactions that significantly alter the oceanic crust and rapidly, become buoyant, and begin their ascent to the
which provide potential energy sources for microbial life. Off- seafloor [Bach et al, this volume]. The high temperatures of