Endeavour Segment

kelley@ocean.washington.edu; jdelaney@u.washington.edu

Hydrothermal BiologicalSystems from the Subseafloor

to the Water Column

James CowenDepartment of Oceanography

University of HawaiiSession #5, 1/11/05

Outline• Geological/geochemistry background—Mike Mottl, Mon.• MOR Hydrothermal Habitats/biogeochem—JPC, Tues.

– Subseafloor– Seafloor– Hydrothermal plumes– MOR magmatic/tectonic events

• Molecular biology primer—Mike Rappe, Tues.• Ridge flanks subseafloor biosphere—JPC, Wed.• Serpentinization and mud volcanoes—MM, Wed.,• MOR hydrothermal microbiology—John Baross, Thurs.• Origin of life—John Baross, Friday

Definitions

• Microbial groups by temperature tolerances– Psychrophiles: optimal growth at -10 to 20 oC– Mesophiles: optimal growth at 10-50 oC– Thermophiles: optimal growth at 40-70 oC– Hyperthermophiles: optimal growth at >80oC

• Redox reactions: In living organisms, chemical energy isstored in high-energy electrons that are transferred fromone atom to another in oxidation/reduction reactions.

NO3- + 2H+ + 2e- NO2

- + H2O H2 2H+ + 2e-

NO3- + H2 NO2

- + H2O

NO3- reduction

Half-cell rxtnsH2 oxidation

G1

Karl 1995

G1

Which potential metabolic processes isenergy-yielding?

– Methogenesis or methanotrophy?– CO2 + 4H2 CH4 + 2H2O– CH4 +2O2 CO2 +H2O

– Sulfur oxidation or reduction?– S(s) +1.5O2 + H2O SO4

2- + 2H+

– S(s) + H2 H2S

Depends on (i.e., Gibbs free energy of reaction, ΔGr)

– Temperature (<150oC for biotic reactions)– Pressure– Chemical composition of system (in solution and

solids)

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Deep-Sea Hydrothermal Systems• Novel communities?

– MOR system 60,000 km, ~60 % hydrothermallyactive!

– Not counting ridge flanks, subduction zone back arcsystems, hotspot volcanism etc

• Key role in origins of life, early earth?– Hot, reducing conditions like early earth– UV protected; refuge from bombardment of

planetesimal bodies– Abundant source of electron donors (e.g. H2)– Presence of electron acceptors (e.g., seawater SO4

-2;Fe+3 from mineral hydrolysis)

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• Analogue for extraterrestrial oceancovered bodies (e.g., Europa)– Probable liquid ocean (tidal heating)– Possible hydrothermal circulation (tidal

heating)– Planetary differentiation (partial melt of

rocky interior??—deep tidal heating)

(Nasa Galileo mission, 1997)

(R. Thomson)

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prec.

leached

Neutrally-buoyant plume

Buo

yant

plu

me

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Hydrothermal Vents

Subseafloor Ecosystems

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MOR hydrothermalcirculation

1-3: Recharge zone•<2-150oC•e- acceptors: O2, NO3

-, SO4-2

•e- donors: Fe+2, org-CSW•Initial water-rock reactions

4-5: Reaction zone•High To (to 400oC), fresh rock at cracking front •Intense water-rock reaction•Volatile/metals leaching•Too extreme for active life

6: Upflow zone•Fluids at 350-400oC; low pH; high reduced metals/volatiles•No active life•Some entrained fluids (w/cells)

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Discharge Zones1. Black Smokers

• 200-400oC (mixingdependent)

• No active microorganisms• Entrained microbes present• High concentrations of

reduced metals/volatiles• Reducing, low pH

2. Diffuse flow• 2 to ~150oC• Chemical disequilibria (High

To fluids + SW mixing)• Microbially dynamic

Active Subseafloor Biocommunity• Intense thermal/chemical

gradients• Tolerable To zones (<150oC)• Includes chimney walls

Rapid venting at 260-400oC

Slower ventingat 30-330oC

G2

Kelley et al. 2002

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MOR subseafloorbiosphere

Kelley et al. 2002

Abiogenic(degassing/fluid-rock rxtns)

Biogenic oxid-reduc rxtnsduring fluid-SWmixing

Chemical transformations in hydrothermal systemsG2

Potential Microbial Metabolic Processes

FermentationOrganic compoundsOrganic compoundsOrganic compounds

S & sulfate reductionOrganic compoundsSo, SO42-Organic compounds

DenitrificationOrganic compoundsNO3-Organic compounds

Methane oxidation?SO42-CH4

MethanogenesisCO2CO2H2

S & sulfate reductionCO2So, SO42-H2

H2 oxidationCO2NO3-H2Anaerobic

Heterotrophicmetabolism

Organic compoundsO2Organic compounds

Methane (C-1)oxidation

CH4, CO2, COO2CH4 (and other C-1compounds

NitrificationCO2O2NH4+, NO2

-

Mn oxidationCO2O2Mn2+

Fe oxidationCO2O2Fe2+

S oxidationCO2O2HS-, So, S2O32-, S4O6

2-

H2 oxidationCO2O2H2Aerobic

Metabolic processC sourceElectron acceptorElectron (energy)donor

Conditions

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e- donors

e- acceptors

Chemical systems

G2

Amend and Shock 2001

‘H-O-N’ Chemical SystemG2

‘H-O-S’ Chemical system

Amend and Shock 2001

G2

370 reactions

>200 ‘species’ currently known

G2

(Kelley et al. 2002)

<1 to >20 m

Hydrothermal vent chimney

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Chimney habitats

Kelley et al. 2002

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Hydrothermal Vents

Seafloor Ecosystems—

–Bathed in warm vent fluids/SW,–Variable To, O2, H2S, etc. (e.g., tides, currents,discharge rates)

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Macrofauna, endosymbiontsChemoautotrophic sulfur and methanotrophic symbionts

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Surface colonization by H2S oxidizing bacterium (Acrobacter sp.) excreting elemental S as rigid irregular filaments

(Taylor et al. 1999)

Microbial matsG1

Fe-encrusting, sheathed bacteria attachedto vestimentiferan worm tubes

Fe hydroxideassoc w/sheath

Fe hydroxide Assoc w/”slime”

Sheathed bacteria

(Juniper and Tebo 1995)

worm tubeouter surface

worm tubeouter surface

Microbial mats:

Fe-deposits often cemented by amorphous silica

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Hydrothermal Plumes

Buoyant and Neutrally-buoyantPlumes

G3

Neutrally-buoyant plume

Buo

yant

plu

me

G3

High buoyancy hydrothermalplume rising into a crossflow

J.W. Lavelle, NOAA

G3

Cowen

G3

(Cowen and Baker, 1998)

2

2

4

2+

2+

222NH4

+ oxid

G3

Microbial processes:•Mostly aerobic (w/ O2)•Low To (<2oC)•Cells free living and•Particle-associated•Microbes likely opportunistic

Plume from single source invariable currents

J.W. Lavelle, NOAA/Seattle

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Plume from multiple sources in variable current - PipeOrgan and neighboring vents - animation

J.W.Lavelle, NOAA

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Implications of studies of hydrothermalplumes

• MOR are 60,000 km long corridor of focuseddeep ocean productivity– Oasis for deep-water zooplankton– Highway for larval and microbial transport– Enhanced biodiversity

• Extraterrestrial search for life– Subsurface basement ecosystems difficult to access– Vent systems relatively small area

• But…the water column more diffuse, butexpanded detection zone

G3

MOR Volcanic EruptionsEvent Detection and Response

(Chadwick et al. 1998)

Old flow New flow

G4

Kelley et al. 2002

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Intrusive dike phase Extrusive

flow

Response to MOR magmatic/tectoniceventsEvent Plume

(Summit and Baross 1998)

(Haymon et al. 1993)

Snowblowerventing

G4

(Baker 1998)

Event Plume: 1996 Gorda Ridge

Massive, catastrophically expulsed volume of hydrothermalfluids—unique chemistry and microbiology, suggesting originsIn portions of subsurface different from those supplying chronic Hydrothermal discharge

10’s kms

1,000 m vertical

G4

Heat from cooling lava

Heat from cooling dike

Pre-existing hotfluids releasedby diking or othermagmatic process(or major tectonic?)

•Not enough heat•Heat released too slow (EPs form rapidly)•Chemistry inconsistent w/ that of EPs (EP: low uniform 3He/heat; low Mn/heat)

•Presence of thermophiles in EPs

(Embley and Lupton 2004) (Summit and Baross 1998)

G4Event PlumeFormation

Magmatic event: heat flux vs time

0 100

5 103

1 104

1.5 104

2 104

2.5 104

3 104

0

2 1016

4 1016

6 1016

8 1016

1 1017

0 0.5 1 1.5 2 2.5 3 3.5

Heat Flux (MW) 1993 CoAxial Floc

Heat Flux (MW) 1993 CoAxial Flow

Heat Inventory (J) 1998 AxialH

eat

Flu

x (

MW

)

Heat

Invento

ry (

J)

Years since eruption

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Real time detection of seismicity associatedwith magmatic/tectonicevents

G4

T-phase waves

(J. Cook 2004)

U.S. Navy’s Sound Surveillance System (SoSuS)

G4

Post-eruption time-seriesvent fluid chemistry

(Huber et al. 2003)

Volatile-rich SW-dominated

G4

(Huber et al. 2003)

Higher To Lower To

Time series rRNA community signaturesG4

Implication of magmatic (tectonic too)events for Microbial Communities

• Changes to hydrothermal circulation– Intensity (e.g., higher/lower flux)– Subseafloor plumbing (e.g., new

cracks/fissures/vents; also demise of whole ventfields)

– Temporal/spatial variability in thermal / chemicalgradients and in microbial consortia

• Event plume formation– Heat and mass flux to ocean– Large-scale dispersion of subseafloor

microorganisms (long-term colonization/survival?)– Window into MOR subsurface biosphere

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Summary• Deep-Sea Hydrothermal Systems

– Global corridor of high productivity and high microbialdiversity (both subseafloor and in water column)

– Diverse habitats• thermal / chemical / substrate gradients• Subseafloor, seafloor, water column

• Important implications for origin of life (stay tuned for Baross lecture-Friday)• Implications for search for life on liquid (esp.

water) / ice covered extraterrestrial body– Habitat (To, chemistry, substrates), metabolic diversity– Initial search strategies

(Kelley et al. 2002)

G4

(Lupton et al. 1998)

Tracking EPs bySeeding with floats (e.g., RAFOS)or AUVs*

*Autonomous underwater vehicle

recovery

launch

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Standing Stock [mg C m-3]Production/(Consumption) [mg C m-2d-1]Flux [mg C m-2d-1] Cowen et al. 2004

G3Preliminary Mass Balance for OC Production

in Hydrothermal Plume

• Analogue for extraterrestrial oceancovered bodies (e.g., Europa)– CO2 + 4H2 CH4 + 2H2O– 2CO2 + 6H2 (CH2O)n + CH4 + 3H2O

In extreme case of limited e- acceptors:– 2Fe(OH)3 + H2 2FeO +4H2O

However,– There is SOx and could be O2– Radiolytic O2:

• 40K ~ 0.012% total K(β-particles and γ-radiation + 2H2O 2H2 + O2)• 1010 moles O2 / yr on Europa107-109 kg biomass / yr (if plenty CO2)105-106 kg biomass / yr (if CO2 limited)

(R. Thomson)

Europa vent fluids too reducing and high pressure: reaction equilibrium to right

Earth’s oceanic production: 1013 kg C yr-1

Hydrothermal production: 107-108 kg C yr-1 (w/O2!)

(Gilmour and Sephton, 2004)

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Pathways and sites for microbial biomass production inMOR hydrothermal system

Karl 1995

--Hypothetical location in hydrothermal system of biomass production

G2

B11

Life: properties-oriented definition

Generational: changes inmineralogy due to change inenvironment and ion source.Individuals: water release /adsorption (clay minerals);outer resistant layers (e.g.,oxide or silicate layers)

Generational: Genetic adaptation,exchange of genetic material.Indivisual: homeostaticadaptation: movement, cellularshrinkage / spore formation innutrient-poor environment

Reaction to,compensation forand develop newabilities to respondto environmentalchanges

Adaptationtoenvironment

Crystals break due tocleavage; cleavage surfacemay contain “growth”information

Various mechanisms (binaryfission); genetic code preservedand duplicated

Multiplication ofinformation

Reproduction

Crystal growth withfavorable environ and ionsources; Local surfacereversibility can correctmistakes during silicate ormetal oxide minerals

Cell growth as long as nutrientsavailable / environ. conditionsfavorable; until reprod occurs;Self-organization, errorscorrected by enzymes

Increase in size ofsingle unit

Growth

Energy uptake via heat /light, elevation of e- tohigher energy bands;

Various types of biochemicalpathways including chemo- andphotosynth; energy stored asATP or GTP

Yield of energy byelectron transfer

Metabolism

Inorganic ParallelOrganic MechanismBasicRequirement

Property

Schultze-Makuch et al. 2002

G1

Definition of Life: Inspired bysearch for extra-earth life

1. Bounded microenvironments inthermodynamic disequilibrium withexternal environment

2. Capable of transforming energy and theenvironment to maintain low entropy*state

3. Capable of information encoding andtransmission

Schultze-Makuch et al. 2002

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*Entropy: The tendency of a system, including the universe, toward increasing disorder and inertness

(Haymon et al. 1993)

Snow blower vents, 9o N-East Pacific Rise

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In situ Chemical Redox Analyzer

dissolved O2, H2S, MnII, FeII, S2O3

2-, S4O62-, Sx

2-, S0, aqueous species of FeIII and FeS

In situ VoltammetricElectrochemicalmeasurements

Volts (vs AgCl)-1.5 -1.0 -0.5

i (A)

-1e-6

0

1e-6

2e-6

time (sec)

0 30 60 90 120 150 180

co

nc

en

tratio

n (

µM

)

0

100

200

300

400

500

Free H2S

SAVS

FeS

A

B

FeSfree H

2S

SAVS

*

Brian Glazer

G3

Thomson et al. 2004

G3