SMS 501 Biological Oceanography 7 October 2009

Lecture 12 Mary Jane Perry

Prokaryotes III – Vents, seeps and other microbial lifestyles

VentsMetabolism (redox reactions)

ConsortiaSymbiosisS and CH4

Biominerals

Microbes transformed the earth (and ocean)

Once ‘life’ started, it transformed the world.

Recall evolution of oxygen (reading assignment)Falkowski and Godfrey (2008)

Electrons, life and the evolution of Earth's oxygen cyclePhil. Trans. R. Soc. B 363, 2705-2716Once ‘life’ started, it transformed the world.

Debate is strong on initiation of life

source of organics:– extraterrestrial– biotic soup (lightening + gases (CH4, NH3 and H2))– hydrothermal vent origin (mantle degassing, heat, pressure

mechanism:– ‘metabolism’ first vs. ‘information’ (RNA) first

Today, vents and seeps as introduction to microbial metabolisms and lifestyles

other than photosynthetic or organo-heterotrophic

Summary: three basic modes of nutrition:

photosyntheticnon-oxygen evolving, anaerobic and aerobicoxygen evolving (cyanobacteria)

chemoautotrophic

organo-heterotrophic – aerobic and anaerobic

…… and combinations thereof

Edwards 2005. TRENDS in Microbiology 13

Some chemical reactions that are major sources of metabolic energy for lithoautotrophs in deep-sea ecosystems

(with representative heterotrophic reactions for comparison)

Jørgensen & Boetius. 2007. Nature Rev. Microbiol. 5: 770

– hydrothermal vents (magma–seawater interactions)– ‘cold’ seeps (high organic deposition w/ microbial transformations)

Tivey 2007. Oceanography 20:50

Also note, thinner sediment overlying spreading centers (less on faster spreading centers; > 80 mm/yr).

Thicker sediment on continental shelves.

black smoker & calcite Lost City

Deep sea hydrothermal communities first discovered near Galapagos in 1975 by geologist – Deep Tow, as a 0.1 ºC temperature anomaly.

Camera revealed piles of dead clams on hard substrate(unexpected large size and high density for deep sea)

Geologists visited Galapagos vents first with ALVIN – 1976Biologists didn’t get there until 1979.

Beggiatoa mats, crab, clam,

vestimentiferan worms

Hydrothermal vent systems vary

associated with slow or rapid spreading center

warm (20ºC, Galapagos) or HOT (> 390ºC, East Pacific Rise)(major sampling challenge)

mineral composition and locationblack smokers – on spreading center, fueled by volcanoes, active or fossil {western Australia - > 3 BY}, water that comes in direct contact with magna chamber, rich in transition minerals, biogenic & abiogenic methane, acidic, archaea growing at temperatures >120ºCcarbonate chimneys {Lost City - only one found {2000}, off-axis of spreading center, alkaline waters, no direct contact with magna, lower temperatures <200ºC, appears to have been functioning for >30,000 yr

microbes – unique; often in consortia; many symbiosis with megafauna (vestimentiferan tubeworms, bivalve mollusks, provannid gastropods, alvinellid polychaete and bresiliid shrimps)

Tivey 2007. Oceanography 20:50

http://en.wikivisual.com/index.php/Black_smokers

Seawater circulation in black smoker

Chemo-auto-trophic metabolism: electron donors from vent waters; electron acceptors from ocean bottom waters

X‑ray fluorescence map collected from weathered-exterior (seawater-exposed) surface of extinct hydrothermal chimney. Iron – red, sulphur – green, silicon – blue; light-green – sulphide minerals. Jorgensen and Boetius, 2007,

Nat. Rev. Microbiol. 5: 770

Martin et al. 2008. Nature Rev. Microbiol. 6: 805

metabolism

Consortia of microorganisms

– control the rates of redox reactions– modify their environment by producing biofilms and mats (or establishing symbioses with animals).

Structure and higher density of mats or films enable them to– avoid being washed away by the currents and – access energy more easily and reliably (in one organism produces substrate for another organism).

Distributions of bacteria and archaea in relation to physical–chemical parameters (temperature, pressure, pH, redox level, etc.) produce gradients in microbial metabolisms and species vs. distance from venting waters (distance often vertical – up a chimney).

Anaerobes closer to venting water; aerobes further way.Autotrophs closer to vents; heterotrophs further away.

Schematic cross-section through hydrothermally active hot spot in Guaymas sediments with 2-layer model for microbial zonation: I) Anaerobic consumers (sulfate reducers, anaerobic methanogens) intercept substrates of thermogenic subsurface origin (CH4, organic acids) near the sediment surface. II) Their metabolic end products (CO2, sulfide, simple organic compounds) are intercepted by the surface Beggiatoa mats.

Amend & Teske (2005) Palaeogeography, Palaeoclimatology, Palaeoecology 219: 13

H2S + 1/2 O2---> So + H2O

Aerobic sulfide oxidation (chemo-auto-lithotrophy)

Heterotrophic sulfate reduction – anaerobic respiration of organic carbon

2CH2O + SO4 2-

2CO2 + H2S + 2OH-

Many chemolithotrophs require both O2 and reduced S (here H2S), they are often found at the interface between aerobic–anaerobic world. In consortium, product of one species is substrate of other.

Consortium – coupling redox reactions:

External consortium with redox S oxidizers and reducersOvermann and van Germerden. 2000. FEMS Microbiol. Review 24: 591

Symbiosis with redox sulphur oxidizers/reducers (vents, seeps) in gutless marine oligochaete, Olavius algarvensis with two endosymbiotic bacteria: sulphate-reducing uses organic C and produces sulphide that serves as energy source for sulphide-oxidizer

Dubilier et al., 2001. Nature 411: 298

Dubilier et al. (2001) Nature 411: 298

gutless marine oligochaete, Olavius algarvensis two endosymbiotic bacteria: sulphate-reducing that produces sulphide that serves as energy source for sulphide-oxidizer

uses organic C and S-oxides; produces H2S

oxidizes H2S andproducesS-oxide

After the vents,S-based symbiotic associations were found in many low O2

environments (seeps, low O2 pockets, dead whale carcasses)

Methane (CH4) production and consumption

Methane (CH4) - climatologically active gas (10 x CO2)

Two sources of methane:

* biogenic production (anaerobic, high organic carbon environments)

* high temperature, abiogenic (thermocatalytic, i.e., in vents)

Think “consortia” – often find consortia of producers (methaogens) and consumers (methanotrophs)

Methane – CH4

Methanogens (methane-producing, anaerobic Archaea); ex:

4H2 + H+ + HCO3- CH4 + 3 H20

CH3COO-+ H2O CH4 + HCO3-

Emission to atmosphere 5.05 *1010 tonnes year (Crutzen, 1991), with equal contributions from:

* natural wetlands* rice paddies* ruminants and termites* coal and gas mining* oceans, freshwaters and biomass burning

Does not include potential contributions from deep biosphere

0.5m

Methanotrophs – methane-oxidizing Eubacteria; use methane as source of energy

Can be coupled to S cycle.

Methane oxidizers reduce emissions.

Think “consortia” – methanotrophs and methaogens

CH2O

Couple with S cycle

Biogenic methane production observed world wide– product of anaerobic decomposition of organics (may be secondary products, such as acetate)– variety of depths, from shallow to deep sea

Methane clathrates high pressures and low temperatures squeeze water and methane into solid form (methane in center ofice cage). 1 L clathrate ~ 168 L gas

http://peggy.uni-mki.gwdg.de/Docs/Kuhs/clathrate_hydrates.html

Methane clathrate Temperature–pressure phase diagramConcern for global warmingClathrate Gun hypothesis for Permian–Triassic extinction

http://ethomas.web.wesleyan.edu/ees123/clathrate.htm and Sibuet and Olu. 1998. DSR 45: 517

Global distribution of cold seeps. Typically ~ 300 m thick. Mainly CH4, but also hydrocarbons and sulfides (depending on the geology). Pore space ofseabed within gas-hydrate stability zone consists of 1–10% gas hydrate on average, resulting in a global gas-hydrate reservoir of 1,000–22,000 gigatonnes of carbon85. Gas hydrates form when gas saturates thepore water at hydrostatic pressures of >60 bar and ambient temperatures of <4°C.

a) Venting methane b) gas hydrate layers

Boetius and Suess. 2004. Chem. Geol. 205: 291

http://www.bubbleology.com/seeps/Seep_Blowout.html

CLATHRATE GUN?

Clathrate Gun hypothesis: Thought to have been triggered by outside warming event, maybe super-volcano; lead to Permian-Triassic extinction

economic value – high temp stable enzymes (fast); new metabolic pathways (remediation, extraction, etc.);

mineral concentrations.

Vents – impact on global trace metal budgets

vents, seeps, etc. – not so rare

Formation of mixed colloids of Mn- and Fe-oxide-hydroxides throughbiogenic oxidation of Mn(II) and abiogenic oxidation of Fe(II). (a) Schematicillustration of the steps leading to the formation of Mn(II) and Fe(III), to Fe(III)-oxide-hydroxides and to Mn(IV)-oxides and, finally, to their respective colloids.These colloids increase in size until mixed colloids, layers of Fe(III)-colloids (pink) and Mn(IV)-colloids (orange) are formed. (b) The formation of Mn-colloids is promoted by endolithic bacteria (ba) that are covered with S-layer. Individual bacteria are decorated with pillar-shaped protrusions (p) that are embedded into the Mn-rich region of the metallic zone (see panel (d)). (c) This polished cut through a nodule shows the concentric arrangement of Fe-rich and Mn-rich layers. Mn: Mn-rich region; Fe: Fe-rich region. (d,e) X-ray mapping of a nodule crosscut confirms that separate layers of Mn (d) and Fe (e) exist. Blue indicates low levels of Mn or Fe and red indicates high levels of Mn or Fe.

H2S eruptions off coast of Namibia

Results in sulfurous smell, dead fish, mobile crustaceans escaping on to beach.

High productivity area. Sedimentation of organics leads to anoxia and ultimately buildup of H2S in bottom sediments.

SeaWiFS ocean color image, from Ward, Oct 2006 Sc. Am

Concept of Deep Biosphere (life below the surface, >3000+m)* pores in rock account for about 3% of Earth’s upper crust* microbes occupy 1% of those pores

Evidence: direct cell counts from the deep-sea drilling bore holes, cells in fluid inclusions, deep aquifers, oil reservoirs, deep rocks, deep marine sediments, fluid emissions from vents, etc. Contamination? Probably not: use of markers; unique genetics

Molecular analysis indicate many are Arachea and are unique to subsurface biosurface

What fuels the deep biosphere? below earth’s surface, T increases w/ depth; abiogenic reduced compounds –> heat & metals. H2 can be abiotically produced via many pathways.

Hypothesis of a H2 – driven biosphere composed of acetate- producing bacteria (H2 + CO2 –> acetate) and methanogens (H2 + CO2 –> CH4 or degradation of acetate –>CH4 )global C in subsurface Prokaryotes (5.18 x 1014 kg) ~ C in terrestrial plants (5.60 x 1014 kg) Whitman et al., 1998, PNAS