Transcript The bioinorganic chemistry of the ancient ocean: The co

Trace Metals and the Ancient Earth:
The Co-Evolution of Life and Earth’s Chemistry
Marine (bio)inorganic chemistry as a tool for deep time studies
Hello, My daughters were very happy and surprise to find a real message in a bottle. Thanks for this magic moment.
we find it on the Trouville Beach (Normandy) the 10 March, 2005 Good luck for your project.
Natacha Rousseau & Chloé et Emma Sbruzzi
Attachment, photo taken of the bottle apparently as it was found (from the shadow it is 7 or 8 o'clock in the morning):
12.755 L08
Canfield, 2005
Outline
Some recent ways inorganic approaches have
contributed to studies of the ancient Earth
•
•
•
•
•
•
Sulfur isotopes (Canfield, Farquar)
Chemical history/modeling (Williams and Da Silva, Anbar and Knoll, Saito)
Metal isotopes in ancient rocks (Anbar, Rouxel, Severmann)
Metal abundances in ancient cores (Anbar)
Genomic studies on extant organisms (Dupont, House, Falkowski, Wolfe-Simon, Ridge)
Physiological studies on extant organisms (Sunda, Morel, Saito, Wolfe-Simon)
What is this field called:
Geobiology, Astrobiology, Origin of Life, Deep time, Microbial Biogeochemistry, Paleo
How do we study life and biogeochemistry
of the ancient ocean?
1.
2.
3.
4.
Microfossils
Organic molecules: biomarkers of life
Isotopes or relative abundances of elements in rocks formed in that time
– Biologically influenced: Sulfur, carbon, iron
– Non-biologically influenced (e.g. platinum group elements, Os, rare earth
elements Nd)
Genomic information ‘preserved’ in extant life
The challenges in acquiring actual information about the ancient Earth:
– Are microfossils really biotic in origin?
– Are biomarkers really made by the organisms we think make them?
– Are there abiotic processes controlling isotopic fractionation as well?
– How do we decipher the information in genomes and proteomes?
– Can information really be preserved in DNA over billions of years?
•
•
•
Lateral gene transfer
Mutation rates
“Genomic Diagenesis”
Current major controversy:
When did O2 arise in the atmosphere?
When did oxygenic photosynthesis evolve?
(Is the house of cards coming down?)
• Microfossils are not reliable, may not be biological, and certainly do
not give phylogenetic information
• Stromatolites: do not require photosynthesis do be produced (early
ocean much closer to saturation, methane oxidizers can produce
them)
• Sulfur isotopes, and iron isotopes
• Biomarkers:
– Eukaryotic specific markers: Sterols (contaminants?)
– Hopanes: 2-methyl-bacteriohopananepolyol believed to be primarily
cyanobacterial.
• But synthesis genes not found in most abundant extant marine
cyanobacteria: Prochlorococcus and Synechococcus
• We don’t know when oxygenic photosynthesis evolved
• Kirschvink’s Snowball Earth Hypothesis: much later ~2.2bya, oxidized
methane and drove the Earth into massive ice age.
The Schopf Microfossils
Another current controversy:
Early or Late evolution of oxygenic photosynthesis
•
•
2.78 billion years ago (early)
~2.3 billion years ago (late)
•
From Koop and Kirschvink:
– “The critical piece of evidence placing the origin of cyanobacteria and locally oxic
environments in the Archean is the discovery in bitumens from rocks as old as 2.78 Ga of
organic biomarkers apparently derived from lipids used by cyanobacteria and eukaryotes in
the cell membranes.”
– “Raymond and Blankenship found that of 473 O2-dependent enzymatically catalyzed
reactions…. 20 have at least one O2 independent counterpart that performs the same
reaction. [BchE does the same rxn as AcsF but uses B12 instead of O2]. The assumption
that sterol synthesis is always O2-dependent and always has been therefore merits close
inspection”.
–
Conclusion, just because something requires an aerobic enzyme now, doesn’t mean
there was anaerobic enzyme that is now extinct.
–
On the flip side, the extant cyanobacteria don’t make the biomarkers attributed to ancient
cyanobacteria (Hopanes: 2-methyl-bacteriohopananepolyol believed to be primarily cyanobacterial. But
synthesis genes not found in most abundant extant marine cyanobacteria: Prochlorococcus and
Synechococcus)
The oldest fossil evidence for eukaryotes and cyanobacteria therefore reverts to 1.78–1.68Gyr ago and
2.15 Gyr ago10,11, respectively. Our results eliminate the evidence for oxygenic photosynthesis 2.7 Gyr ago and
exclude previous biomarker evidence for a long delay ( 300 million years) between the appearance of oxygenproducing cyanobacteria and the rise in atmospheric oxygen 2.45–2.32Gyr ago1.
Brocks Goldschmidt talk summer 2009:
Reinterpretation of organic biomarker record such that Eukaryotic life evolved after the Great Oxidation Event (which
occurred at ~2.3 bya)
Sulfur isotopic record
• Sulfur fractionations are greatly reduced at low concentrations of sulfate (<200uM)
• Bacterial Sulfate Reduction (BSR) fractionate between 20-40% of d34S at high sulfate
• Explanation – low atmospheric oxygen concentrations cause low pyrite (FeS)
weathering rates, resulting in a small sulfate inventory in the early ocean
Canfield, 2005
The Canfield Ocean:
Canfield, 2005
Much higher Si in ancient ocean
High Si causes decrease in P adsorption to iron oxides (BIFs)
Causes an underestimate of ancient P abundances
Iron isotopes (fractionation is strongly influenced by redox)
(Low iron at <1.6 billion years = small fractionations)
oxide
pyrite
Metal concentrations
in ancient cores
Can we see a signal inside extant microbes?
“While it would appear that the solvent for life has
always been water, other conditions, such as those
of temperature and the dominant chemical species
in the atmosphere, have changed with time. Life,
while itself producing many of these changes, has
evolved with the changes. … We must note too
that the changes in the atmosphere and the
consequent changes in the sea and in the earth’s
surface over millennia have had a considerable
effect especially on rare element distribution and
uptake. Some of the elements found in
biology were selected a long time ago,
in very different circumstances.”
(Fraústo da Silva and Williams, 1991)
Distinct Trace Metal Physiologies:
Marine Cyanobacteria versus Eukaryotic Phytoplankton
Phaeocystis antarctica
Prochlorococcus
0.5
-1
0.05
12
11
12
13
-10.5
-11.0
0.1
-11.5
0.0
-11.0
-12.0
-11.5
13
T1 Growth Rate
p(Co 2+)
(Saito et al., 2002, L&O)
T2 Growth Rate
-12.0
log C
o
-12.5
-12.5
2+
-13.0
-13.0
(M)
(Saito and Goepfert, submitted)
)
p(Z 2+
n )
11
0.10
0.2
(M
0.15
0.3
2+
0.20
0.4
Zn
0.25
log
0.30
0.00
)
Growth rate (d
0.35
ATE
GROWTH R
-1
(d )
0.6
Cobalt-zinc substitution also observed in coccolithophores and diatoms
(eukaryotic phytoplankton)
Emiliania huxleyi
1.00
0.75
-10
-11
-12
log Co 2+
(M
Zn
0.00
-8
-9
-10
-11
-12
-13
-14
2+
0.25
)
0.50
-13
(M)
-14
log
gZ
n
2+
(M
)
-11
-1
)
(d
E
T
A
R
GROWTH
1.25
Sulfur isotope data:
The oceans were reducing and sulfidic
from 2.5 to 0.543 billion years ago
(Canfield, 1998; Anbar and Knoll, 2002)
• Low sulfide in Archean due to High Fe
• O2 production causes increased S weathering
and oceanic S inventory increase
• Bacterial Sulfate Reduction converts
much of sulfate to sulfide
The Proterozoic Bioinorganic Bridge
Low Mo, Cu, Zn, Cd
O2
Oxidize CH4 cause
snowball Earth?
SO42-
Oxygenated layer
Deep reduced layer
SO42-
BSR
H2S
Assumptions
• Evolution of bacterial sulfate reduction must be ancient
• Timing and “resistance” of geosphere to oxidation by oxygen – fast or slow?
• Oxidation rates of metal-sulfide complexes in a thin oxygenated upper water column
– fast or slow relative to growth rates?
• When did oxygenic photosynthesis evolve? Cyanobacteria tree with chloroplasts,
believed to be the first to have this capability.
• When did eukaryotic life arise? 2.7 bya? Contamination. Much more modern?
1.8bya for first simple fossils, and diversity of animals as late as 0.6bya.
Sulfur isotope data:
The oceans were reducing and sulfidic
from 2.5 to 0.543 billion years ago
(Canfield, 1998; Anbar and Knoll, 2002)
• Low sulfide in Archean due to High Fe
• O2 production causes increased S weathering
and oceanic S inventory increase
• Bacterial Sulfate Reduction converts
much of sulfate to sulfide
The Da Silva-Williams vs. Canfield Paradox:
Oxygenation of the Earth is caused by the
cyanobacteria. Yet numerous results are
consistent with their evolution in a sulfidic
ocean
How could the cyanobacteria have
evolved in a sulfidic ocean, if they are the
mechanism for making the ocean
sulfidic?
 Modeling bioactive trace elements:
using recent thermodynamic data
 Solubility and aqueous complexes
Saito, Sigman and Morel, Inorganic Chimica Acta 2003
Influence of increasing sulfide concentrations on Fe, Mn, Ni, Co, Cd, and Cu
A.
1e-7
2+
Fe
1e-8
Mn2+
1e-9
1e-10
Ni2+
1e-11
Co2+
1e-12
Log Concentration (M)
Log Concentration (M)
1e-6
1e-13
1e-8
1e-7
1e-6
1e-5
1e-4
1e-3
1e-5
1e-6
1e-7
1e-8
1e-9
1e-10
1e-11
1e-12
1e-13
1e-14
1e-15
1e-16
1e-17
1e-18
1e-19
1e-20
1e-21
1e-22
+
B.
FeHS
CoHS+
1e-8
1e-7
C.
1e-8
Zn
2+
Co
2+
Cd
2+
Cu
+
Cu2+
1e-7
1e-6
1e-5
Log [HS-Total] (M)
1e-6
1e-5
1e-4
1e-3
Log [HS-Total] (M)
Log Concentration (M)
Log Concentration (M)
Log [HS-Total] (M)
1e-6
1e-7
1e-8
1e-9
1e-10
1e-11
1e-12
1e-13
1e-14
1e-15
1e-16
1e-17
1e-18
1e-19
1e-20
1e-21
1e-22
1e-23
1e-24
1e-25
1e-26
1e-27
1e-28
MnHS+, NiHS+
1e-4
1e-3
1e-6
1e-7
1e-8
1e-9
1e-10
1e-11
1e-12
1e-13
1e-14
1e-15
1e-16
1e-17
1e-18
1e-19
1e-20
1e-21
1e-22
1e-23
1e-24
ZnS(aq)
D.
1e-8
Cd-sulfides (aq)
Cu(II)-sulfides (aq)
1e-7
1e-6
1e-5
Log [HS-Total] (M)
1e-4
1e-3
1e-3
1e-5
HS-
1e-4
Log Concentration (M)
What does a ferrous iron
dominated ocean do to
trace metal abundances?
Log Concentration (M)
A.
1e-5
1e-6
Fe2+
1e-7
1e-8
1e-9
1e-10
FeHS+
1e-6
1e-7
1e-8
1e-9
1e-8
1e-7
1e-6
1e-5
1e-4
1e-3
1e-8
1e-7
2+
Log Concentration (M)
Log Concentration (M)
Mn
Ni2+
1e-9
Co2+
1e-10
1e-4
NiHS+
+
1e-11
1e-3
MnHS
1e-9
D.
CoHS+
1e-10
1e-11
1e-8
1e-7
1e-6
1e-5
1e-4
1e-3
1e-8
1e-7
Log [FeTotal] (M)
E.
1e-8
Co
2+
Cd2+
Zn2+
+
Cu
Cu
1e-7
1e-6
2+
1e-5
Log [FeTotal] (M)
1e-6
1e-5
1e-4
1e-3
Log [FeTotal] (M)
1e-4
Log Concentration (M)
Log Concentration (M)
1e-5
1e-8
C.
1e-7
1e-8
1e-9
1e-10
1e-11
1e-12
1e-13
1e-14
1e-15
1e-16
1e-17
1e-18
1e-19
1e-20
1e-21
1e-22
1e-23
1e-24
1e-25
1e-26
1e-6
Log [FeTotal] (M)
Log [FeTotal] (M)
1e-8
Assume:
pH= 7.5
All metals (except iron) = 10-8 M
50 mM total sulfide
DIC = 0.05M (~double present value
based on ~20 increase in pCO2)
B.
1e-3
1e-6
1e-7
1e-8
1e-9
1e-10
1e-11
1e-12
1e-13
1e-14
1e-15
1e-16
1e-17
1e-18
1e-19
1e-20
1e-21
1e-22
1e-23
1e-24
1e-8
ZnS(aq)
F.
Cd-sulfides (aq)
Cu(I)-sulfides (aq)
Cu(II)-sulfides (aq)
1e-7
1e-6
1e-5
Log [FeTotal] (M)
(Saito, Sigman and Morel, Inorganica Chimica Acta, 2003)
1e-4
1e-3
1e-2
Approximate Concentrations (M)
Archean
Proterozoic
Modern
1e-3
1e-4
1e-5
Dissolved
Oxygen
Iron
Sulfide
1e-6
1e-7
1e-8
1e-9
1e-10
1e-11
1e-12
Approximate concentration of Mn+
3
2
1
0
Approximate Time (billions of years ago)
1e-3
1e-4
1e-5
1e-6
1e-7
1e-8
1e-9
1e-10
1e-11
1e-12
1e-13
1e-14
1e-15
1e-16
1e-17
1e-18
1e-19
1e-20
1e-21
1e-22
1e-23
1e-24
1e-25
1e-26
Archean
"ferro-sulfidic"
Proterozoic
"sulfidic"
Modern
"oxic"
Fe Ni Co Mn Cu Zn Cd
Fe Ni Co Mn Cu Zn Cd
Fe Ni Co Mn Cu Zn Cd
Saito, Sigman, and Morel, Inorganica Chimica Acta 2003
1e-2
Approximate Concentrations (M)
Archean
Proterozoic
Modern
1e-3
1e-4
1e-5
Dissolved
Oxygen
Iron
Sulfide
1e-6
1e-7
1e-8
1e-9
1e-10
Green Algal Family
Diatoms and
(Chlorophyceae and Coccolithophores
Prasinophyceae)
Cyanobacteria
1e-11
1e-12
Approximate concentration of Mn+
3
2
1
0
Approximate Time (billions of years ago)
1e-3
1e-4
1e-5
1e-6
1e-7
1e-8
1e-9
1e-10
1e-11
1e-12
1e-13
1e-14
1e-15
1e-16
1e-17
1e-18
1e-19
1e-20
1e-21
1e-22
1e-23
1e-24
1e-25
1e-26
Archean
"ferro-sulfidic"
Proterozoic
"sulfidic"
Modern
"oxic"
Fe Ni Co Mn Cu Zn Cd
Fe Ni Co Mn Cu Zn Cd
Fe Ni Co Mn Cu Zn Cd
Saito, Sigman, and Morel, Inorganica Chimica Acta 2003
Anbar 2008 Science
Geochemical modeling (including metal-sulfide complexes):
• Iron dominated Archean ocean has a similar chemistry to a Proterozoic
sulfidic ocean: ~10-6M sulfide is enough to control speciation
• Relative abundances: Mn,Co,Ni,Fe(II)>>Zn,Cd,Cu
• Speciation was likely as important as solubility
The trace metal physiology of marine cyanobacteria appears to be consistent
with their evolution in an ancient sulfidic ocean:
Absolute requirement for Co (Sunda and Huntsman, 1995; Saito et al., 2002)
Small zinc requirement relative to eukaryotic phytoplankton (ibid)
Very sensitive to Cd toxicity (Saito, Sigman, Morel, 2003)
High iron requirement (Raven, 1999; Berman-Frank, 2001)
Some sensitivity to Cu toxicity (Brand et al., 1986, Mann et al., 2002)
Abundant Prochlorococcus in low light suboxic zones (Goericke et al,. 2000)
Abundant Nickel Superoxide Dismutase in the Synechococcus Proteome
(Saito and Bertrand, unpublished data)
Station 11 - CRD05
How would these vestigial traits persist
in the modern ocean?
0
Total Cobalt
Labile Cobalt
20
The production on metal-binding
ligands : CoL, NiL, CuL, FeL, ZnL, CdL
Depth (m)
 Biosynthesis of these organic ligands
could have evolved to replace sulfide
ligands and maintain a similar seawater
chemistry.
40
60
80
100
120
140
0
50
100
150
Co Concentration (pM)
200
Genome/Proteome Approaches
to studying the Ancient Earth:
•
•
Whole organism elemental composition analysis:
– Quigg, Falkowski et al., 2003. Ho et al., 2003
Genomic and proteomic analyses (whole organism versus focusing on specific
metalloenzymes:
Whole:
– Zerkle, House, Brantley. Am. J. Sci 2005 (whole)
– Dupont, Palenik et al (PNAS 2007) (whole)
Specific:
– Gamma carbonic anhydrase (Smith and Ferry)
– Superoxide Dismutase (Wolfe-Simon)
– Nickel Famine of Ni requiring metalloenzymes in methanogens
– Rubisco (nonmetalloenzyme)
– Vitamin B12
Quigg, Ho, Morel, Schofield,Falkowski et al.,
Approach:
Grow a large number of
phytoplankton strains in a single
media and measure cellular
metal content for comparison
and statistical analysis.
Major problem with studies like
these:
Measured cellular metal content
(quotas) DO NOT represent a
biochemical requirement
Luxury uptake of metals occurs
Also, using current gene models
and protein family information –
doesn’t take into account novel
metalloenzymes that likely exist.
These experiments pick a
“representative” (arbitrary!) metal
concentration for the media –
directly affects the metal Quota (Q)
•
Michaelis-Menten uptake kinetics

•
 max S 
K   S 
Monod Growth Rate Expression
(completely empirical)

•

Q
 max S 
Q
K m  S 
Relationship between cellular
Quota, uptake, and growth rate

Q




Similar Genome/Proteome approaches:
• Elemental composition analysis:
– Quigg, Falkowski et al., 2003.
• Genomic and proteomic analyses:
– Zerkle, House, Brantley. Am. J. Sci 2005
• “Model metallomes”
– “We calculated model metallomes for 52 prokaryotes based on
the number of atoms of trace metals required to express one
molecule of each metallo-enzyme coded for in the
corresponding genomes. Our results suggest that the use of
metals in prokaryotes as a group generally follows the
hierarchy: Fe >>Zn>Mn>>Mo, Co, Cu, >> Ni, > W, V
– Dupont, Palenik et al (PNAS in press)
Especially obvious with the small Zn proteins : “Zinc fingers”
Eukaryotes
“We hypothesize that these conserved trends are proteomic imprints in
trace metal bioavailability in the ancient ocean that highlight a major
evolutionary shift in biological trace metal usage”
Dupont et al., 2006
Focusing on Specific Metalloenzymes:
The evolution of carbonic anhydrases
•
•
•
•
•
a - Mammalian (Zn, relatively modern)
b - Plant-Bacterial (Zn) ancient too divergent for clock
g - Archaeal, bacterial >4 bya (Fe?)
d - Eukaryotic (Diatom, Co-Zn) limited data
e - Eukaryotic (Diatom, Cd) limited data
Smith et al, PNAS, 1999
Focusing on SuperOxide Dismutases, Wolfe-Simon
Changes in Nickel supply as recorded by BIFs
Evolution of a biochemical pathway
Evolution of
selfish genes
Evolution of
bacterial taxa
Extent of gene transfer
•
•
•
•
The cobalamin biosynthesis genes are spread throughout the marine cyanobacterial
genomes (no clear operons)
Gene transfer occurs, (viral transfer: a cob gene in Prochlorococcus phage)
Ecology demands: cannot lose a piece of B12 synthesis pathway
Environmental separation: Surrounded by other cells that are similar, not by cells with
aerobic pathway
This approach of examining the evolution of specific
enzymes also applies to non-metalloenzymes: e.g. Rubisco
Phil Tortell, L&O 1999
Another problem with genomic approach: extinction of pathways (!?)
Conclusions: the potential for Marine Bioinorganic Chemistry to
contribute to deep-time studies of the Earth
Approaches:
•
Isotopic records (S, Fe, Mo, Cr, others?)
•
Chemical records (Fe, Mo, Ni)
•
Chemical modeling based on 1) geochemical records of major controls or 2) on genomes and
protein coordination chemistry
•
Physiological studies of extant organisms
•
Genomic studies of metalloenzymes
•
Studies of evolution of specific metalloenzymes
•
Combining multiple approaches to piece together a story
Some Observations:
•
Evidence of changes in ocean chemistry/co-evolution of life and biogeochemistry? Geochemical
modeling solves disagreement between S isotopic and phytoplankton physiological data.
•
Physiological characteristics of the Cyanobacteria are consistent with their evolution in an ancient
ferro-sulfide-influenced ocean
•
A nickel famine of methanogenesis
Overall
•
There is potential for utilizing information “stored” in modern organisms to understand the
evolution of biogeochemical cycles, despite the potential for “Genomic Diagensis”