Isotope fractionations in the terrestrial carbon cycle: A brief over view

Adv.

Space

Res. Vol. 15, No. 3, pa. (3)441-(3)449, 1995 Copyright Q 1994 COSPAR Printed in Great Britain. All rights reserved. 0273-I 177/95 $7.00 + o.oa

ISOTOPE FRACTIONATIONS IN THE TERRESTRIAL CARBON CYCLE: A BRIEF OVERVIEW M. Schidlowski Mux-Planck-lnstitutfiirChemie(Otlo-Hahn-lnstitut),D-55020 Muinz, Germany

ABSTRACT The bias in favour of isotopically brought

about

an isotopic

light carbon

disproportionation of “C

global scale, causing an enrichment accumulation pool.

of the heavy complement

As a result,

the terrestrial

branch

of isotopically

carbon

(mostly

terrestrial

species

in the residual

The isotopic

carbon

(mantle-derived) carbon

branch disparity

cycle

since

the time

has

carbon

on a

(inorganic)

comprising

carbon

an organic

made up of “C-enriched between the two principal

back over 3.8 Gyr of Earth

of the carbon

fixation

and a concomitant

oxidized

cycle has gone bipartite,

and an inorganic

can be traced

modulation

of primordial

(‘“C)

carbon

carbon,

in biological

in reduced (biogenic)

in the form of carbonate).

carbon

a biological

light

inherent

history,

of formation

attesting

to

of the oldest

sediments.

INTRODUCTION A conspicuous of terrestrial the

feature carbon

boundary

sedimentary)

of the global carbon

residing

between

the

compartment

Earth’s

crust

This

(1) as oxidized

bipartition

features

holds throughout for volatile

components

the heterogeneous

prominently

and the organic

carbon interface

bipartition discontinuity”

of the totality which marks

In both

the

reservoir

(comprising

typically

crustal

(basically the triad

occurs in two different forms,

and (2) as reduced

in any operational

or biogenic

carbon.

model of the cycle (Fig.1)

to the atmosphere

(if allowance

and

is made

aerosol).

of the oxidized

equilibrium

exchange

the element

carbonate)

fr om the mantle-crust

organics

The principal

(mostly

“Mohorovicic

and mantle.

and in the surficial

of atmosphere-hydrosphere-biosphere), namely

cycle is the glaring

above the so-called

(inorganic)

carbon

branch

are the members

of

system

co %w = COZ(~)= HCO,(,,)= CO:(,,,).

131441

(1)

(3)442

M. Schdlowski

surficial exchange marine

bicarbonate

I

IWO;

reservoir

standing

I- 1 %o 1

I-1O”g

biomass

L

carbon]

[-26%01

It 0 %o 1

SURFACE CRUST crustal

stone,

(sedimentary) reservoir

dolomite)

[-102*g carbon]

\

I

/

CRUST MANTLE

Fig.

1.

Box

mantle

model

reservoirs.

approximately

of the terrestrial Proportions

to scale;

Note that the standing carbon

dioxide

burden

of dissolved

subject

to a kinetic

biomass

enters carbon

the

mantle.

carbon,

as limestone (C,,,)

Fluxes

and

dolomite.

end-product

former organisms

(juvenile)

carbon

time,

crustal

the

The

reduced

as sedimentary

carbon

alteration

of their metabolism

are

accumulation

carbon

channel

of

in marine

from the surface between

the two

for the transfer

originally

carbonate

organic

the ocean’s

retained

sink has taken

or

of the diagenetic

and the products

than

into the biosphere

difference

dioxide

organic

are

boxes).

an effective

it in the form of sedimentary

exists preferentially

polycondensed

of the cycle (circled

had p rovided

geologic

and organic

units)

and the atmospheric

basically

the isotopic

and

are given in brackets.

smaller

carbon

(‘“C)

crustal

(rectangular

res p onsible for a preferential

propagating

by Eq.(l)

storing

pathways

surficial,

reservoirs

of magnitude

flux of carbonate

sediments,

Over

equilibria

showing

of inorganic

with the heavy complement

of the bulk of primordial

Earth’s

oxidized

represented

cycle

compartments

two orders

species into the rock section

The system the crust

about

A continuous

undirectional

of individual

isotope effect (KIE)

newly formed

exchange

--+

is about one order of magnitude,

bicarbonate.

12C in organic matter, bicarbonate.

of surficial

613C averages

reservoir

carbon

e

(Ccarb),

(biologically (“kerogen”), of organic

degassed care

to

from

of most

of

preferentially

derived)

moiety

the acid-insoluble, debris

derived

from

[l]. As was the case with carbonate

Isotope Fractionations carbon,

the organic moiety has also continuously Together,

sediment a.

both

carbon

species

order of 10z2 g C each, with Ccsrb about comparison, ocean

the totality

and biosphere)

one thousandth

of carbon

amounts

of all carbon

ISOTOPIC The observed additionally carbon.

accentuated

bicarbonate

other

hand,

primordial

mantle

primordial

organic

carbon

carbon

degassed

rise to an isotopically constraints

The

It

is well

to a large-scale aspects

mass balance,

most

=

microorganisms. widest

sense,

a result

carbon

today

that

Incorporation

of both With

biochemical

generally

constituting rather

when organic

matter

flux of

to the Earth’s

upper

giving ultimately l&hJ organic

process

are defined by the

(2)

agent

ISOTOPE

responsible carbon

on Earth.

species

and kinetic

that

effects.

is the fraction

for

Biological

the

wholesale

as the

sizeable

imposed

and

in the

fractionations

on the principal

as

metabolic

and living

rapid cycles of anabolism isotope

carbon

by plants

processing

isotope

enzyme-controlled,

most biological

isotopic

quantitatively

or “autotrophic” ion (HCO,)

and/or biochemical

entail

effects

largely

FRACTIONATIONS

fixation

of COz and bicarbonate

reactions

is incorporated

carbon

carbon.

dynamic states undergoing

than equilibrium

lying

On the

R)613Ccarb,

CARBON

the

carbon

it has come to be widely accepted kinetic

1).

the upward

disproportionation,

(1 -

into living systems,

inorganic

thermodynamic

pathways.

the carbon

and an isotopically

is biological

process

the assimilation

of these

that

moiety

Fig.

and R = Corz/Cprim = COrg/(Corg +C&,)

carbon

biochemical

of the oxidized

marine

carbonate

had, upon entry into the atmosphere-oceanisotopic

R613C,,g +

OF TERRESTRIAL

is primarily

(between

shell (between

-25 “/oo (cf.

of this fractionation

ORIGIN

important

fixation

states is

i.e.,

ending up as organic

of terrestrial

for just

oxidation

reservoir

doubt

supplied

fraction

carbon

established

fractionation

accounting

by 61sC values around -5 “/oo. This would imply that all

quantitative

where Cprim = primordial

little

In

(atmosphere,

between reduced and oxidized

around

[3] leaves

had originally

~lSCprim

of primordial

carbon

evidence

heavy carbonate

of an isotope

disparity

with the 61SC-values

from the mantle

been subjected

complement.

isotopic

C&s [cf.2].

CARBON

in both the surficial exchange

carbon),

that

l),

into two species of different

and in the sedimentary

available

than

on the

discontinuity.

biomass)

was characterized

crust system,

carbon

reservoirs

reservoir

OF TERRESTRIAL

and those of reduced

currently

compartments

above the Mohorovicic

by a conspicuous

and the standing

close to zero permil

exchange

to some 1O1s g only (see also Fig. residing

is apparent

rock and sedimentary

four times more abundant

stored in the surficial

of terrestrial

This disparity

entered the crust as part of newly-formed

have piled up sedimentary

GEOCHEMISTRY

splitting

(3 1443

systems

and catabolism,

fractionationa

are due to

Since these fractionations are basically retained in sediments, the above effects are propagated into

(3)444

M.Schidlowski

the rock section of the geochemical

cycle where they have left their signatures

carbon

the beginning

inventory

as from virtually

In the following, that

a summary

have left their imprint

previous

statements

imposed

isotope

will be given of biologically

mediated The

of the subject

the photosynthetic carboxylation a carboxylic

acid (cf.

of a specific

isotope

are supposedly distinct

primary

Fig.

essential

ISOTOPE

of the

reaction

light

2.

stands

stippled:

isotope

active

(‘“C)

Carbon

sites,

Fig. 2 is a synopsis of the principal photosynthetic)

carbon

fixation.

C02).

to be small,

at the limit

In contrast,

fractionations

much larger,

though

the quantitatively [10,11,13].

The kinetic

biomass

“internal”

variable,

most important

Thus the contemporary

(black:

processes;

kr - kd:

matter

relative

enzymatic

feeder

on its way to the to R-COOH

carboxylation

that

reaction.

In

of the light carbon

box.

steps in autotrophic (principally themselves as a sizeable negative

effect in the initial

lying mainly

(atmospheric)

COs(i)

accumulation

in the right-hand

to the feeder substrate diffusion

equal to the value for CO2

in subsequent

distinctly

COz-fixation

reverse

transformed

enzymatic

isotope-discriminating In sum, these express

isotope

being

and

/

dioxide from the external

and is subsequently

shift of the 6r3C values of biosynthesized atmospheric

in favour

among isotopically

in biological

and other

bring about a preferential

in the synthesized

group of

(121.

V

steps

dissimilatory

of the first COs-fixing

sum, these transformations isotope

enzymatic

use bicarbonate,

exchange

and proteins

the living tissue to become

for the product

that

fix

car boxylat ion decarboxylation

rate constants).

photosynthetically

that

carbon dioxide to

that also discriminate

L

isotope-discriminating

pool [C!Os(,,] enters

organisms

into the carboxyl

pathways

/

v

reactions;

corresponding

are preferentially

and the fnst irreversible

fractionation8

in alternative

in inter- and intramolecular

Principal

isotope

of autotrophic

diffusion

assimilatory

carbon

centres,

such as lipids, carbohydrates

\.

Fig.

FRACTIONATION

dioxide is incorporated

2). Equilibrium

fiactionations

draws in full on

[4,5,6,7,8].

metabolism

by which carbon are important

metabolites

isotope

discourse

Th ese are the uptake and diffusion of external

or chemosynthetic

reaction

cycle.

by the author

in favour

in the

COs [9,10,11].

carbon

OF CARBON

fractionations

on two steps

atmospheric

record.

on the global

BIOCHEMISTRY Kinetic

of the geological

in the crustal

diflusion

carboxylation

(mostly

step has been shown in air (-4.4

reactions

O/oo).

are usually

in the range of -20 to -40 “/oo for

ribulose-1,5-bisphosphate (RuBP) csrboxylase reaction biomass bears, in essence, the isotopic signature of C3

lsocope Fractiooations

(3WS

photosynthesis (cf. Table 1) characterized by this siseable isotope effect exercised by the key enzyme of the Calvin cycle that channels most of the carbon transfer to the living realm, with a resulting 619Corg range of about -26 f 7’/00. As a whole, the Earth’s standing biomass is thus markedly enriched in isotopically light carbon relative to the inorganic carbon pool of the ocean-atmosphere system, as evidenced by its principal 61s C erg spread between -20 and -30 O/o0 (Fig. 3). Gross fractionation6 may vary over a considerable range according to which step in the assimilatory pathway (cf. Fig. 2) is rate-controlling, the carboxylation option used (Table l), and how effectively the isotope fractionations are counteracted by those of the reverse (dissimilatory) processes; the highly variable interactions of these processes express themselves differently in different types of plants and autotrophic microorganisms (Fig. 3)

613C [ %o, PDB - 40

- 30

- 20

]

- 10 marine carbonate

- 40

- 30

-20

0 1

-

Fig, 3. Carbon isotope spreads of major groups of higher plants and autotrophic microorganisms that figure as principal primary producers in the present biosphere (triangles denote approximate means). Respective spreads of oxidized carbon compounds in the surficial environment (COz, HCO,, CO:-) are shown in black. The consistently negative 6rsC ranges of biogenic materials imply an enrichment in light carbon (‘“C) relative to the inorganic feeder species (mostly COz). Note that the positive extremes shown for methanogens were obtained in culture experiments under specific conditions that are irrelevant for natural communities.

Most carbon transfer from the nonliving to the living world proceeds by the ribulose1,5-bisphosphate (RuBP) carboxylase reaction (Table 1, reaction 1) which feeds CO2 directly into the Calvin cycle, the principal biochemical mechanism for reducing CO2 to carbohydrate. Since the carboxylation product generated ill this process is a compound

M.Schidlowski

(3446

TABLE

1 Principal

in the Buildup Note that reduction

of CO2 primarily

such as phosphoglycerate (acetate, reaction

Carboxylation

Biomass.

C4 compounds

A). The quantitatively

carboxylase

reaction

Reactions

Abridged

Involved

from [7].

gives rise to C3 compounds

and pyruvate),

acetyl coenzyme

is the RuBP

COz-Fixing

of Terrestrial

(with 3-carbon

(oxaloacetate)

most important

skeletons

and C2 compounds

enzymatic

carboxylation

(1) of the Calvin cycle that forms the initial carbon-fixing

in C3 photosynthesis.

(1) CO, + ribulose-l$bisphosphate -t phosphoglycerate Operates in: C3 plants*, photosynthetic bacteria trophic bacteria.

algae*, cyanobacteria*, purple (Chromatiaceae)*, chemoauto-

(2) COJHCO; + phosphoenolpyruvate/pyruvate -+ oxaloacetate Operates in: C4 plants*, CAM plants*, anaerobic and facultatively anaerobic bacteria. C4 and CAM plants combine this carboxylation with reaction (1). coenzyme A (3) CO, + COZ --, acetate/acetyl Operated in: Green photosynthetic bacteria (Chlorobiaceae)* [primary CO, fixation is by succinyl coenzyme A and a-ketoglutarate]; anaerobic bacteria, methanogenic bacteria*t. A -, phosphoenolpyruvate/pyru(4) CO,+ acetyl coenzyme vate Operates in: Green photosynthetic bacteria (Chlorobiaceae)*, combined with reactions (3) and (2); autotrophic sulphate-reducing bacteria, methanogenic bacteria*t. * Groups of organisms for which carbon isotope fractionations known (see also Fig. 2).

are

t Primary CO, fixation probably by Cl-acceptors; details of the assimilatory pathway of methanogens are poorly known as yet, but the presence of both a-ketoglutarate and pyruvate synthases suggests that reactions (3) and (4) are involved. with a 3-carbon

skeleton This

C3 photosynthesis. eukaryotic termed

(phosphoglycerate), sequence

C3 plants

(Table

1, reaction

responsible

is a relatively specific

[15] and,

late

atmosphere their

photosynthetic [16,17]

Succulent span

sulphur

approaching

less important carboxylic

coupled

by all green plants,

carboxylation

reaction

in C4 plants

designed

of flowering

plants with crassulacean carboxylase spreads

plants

(Chlorobiaceae)

biomass

albeit

(Fig.

3);

carboxylation

(Table

1, reaction

unique

and is based

to photosynthetic

they

rely

is on a

effects of

is lost to the (CAM)

at different

of C3 and C4 plants have a consistently

a

C4 pathway

the unfavourable

of C4 plants

a pathway

entails

bicarbonate, The

acid metabolism

reactions,

for fixing

ion that serves

heavy 3).

are

carboxylase

This process

(Fig.

to counteract

and PEP

(PEP)

to the bicarbonate

use of isotopically

the combined range

(oxaloacetate).

where part of the newly generated

bacteria

the

the

of “C

in the evolution

ferredoxin-linked

acid cycle,

with

leaf anatomy

by both the RuBP compositions

less important

a C4 compound

enrichment

in C3 plants,

as COZ.

is operated

has been termed

green plants relying on it entirely

-2 and -3 ‘/oo relative

achievement

(compartmented)

photorespiration carbon

of between

for the relative

pathway

C4 plants that use phosphoenolpyruvate

2) to synthesize

species

assimilation

bacteria;

A q uantitatively

[14].

minor fractionation as feeder

of carbon

algae and most photosynthetic

CO2 is found in the so-called

the corresponding

can fix times,

so

(Fig. 3). Green low fractionation

on a quantitatively

3) within

prokaryotes

the reductive

[18].

Diffusion-

Isotope Fractionatious

limited autotrophic [19,20] entail

pathways

global isotope

budget

because

SYNOPSIS With this background carbon

cycle (Fig.1)

distributions. obviously

preferentially

small fractionation8

operated

by aquatic plants and microorganisms

(-4 “/oo and less) and make virtually

OF GLOBAL

information

CARBON

ISOTOPE

via the C3 pathway

and the RuBP properties

carboxylase

biomass

as a whole.

signature

of C3 photosynthesis

Ever since then, organic

of C3 photosynthesis imparting -26’/00.

has been

to the reservoir

constituents

gives testimony Cretaceous)

that

isotope

budget.

to the formidable

kinetic

the living realm, bicarbonate difference atmospheric carbonate the CO,

$6

- CO:-

(lzC- enriched)

in the

atmospheric

surficial

COz-burden

of biologically

mediated

biosphere,

Eq.1)

marine

system

+l

Marine reservoir

by almost

on a global

bicarbonate

isotope

enters

“heavy”

as it surpasses

the

late (end-

network

impact

fractionations carbon scale.

of

dioxide The largest

exists

between

solid (sedimentary)

1 and 3).

In general,

complement

of

the bulk of inorganic carbon

content

of the

[cf. 271.

of the global carbon cycle and its glaring display fractionations

(cf. Fig.1)

reflect

the impact

making the carbon cycle the very paragon of a biogeochemical

cycle within the broader

record

a negligible

carbon

represents

two orders of magnitude

bipartition

geological

temperatures)

the latter

rocks

isotopically

2) as a relatively

O/o0 (see Figs.

makes up the residual

exchange

carbon

bicarbonate;

shell,

of sedimentary

mediated)

surface

a

value close to

The fact that

[25,26] in the inorganic

are negligible

3.5

typical

sedimentary 6i3C

has as yet exercised

enzymatically

shift of just

biomass.

In sum, both the characteristic terrestrial

(mostly

(cf.

composition

in the youngest

1, reaction

and +8 “/oo at terrestrial

COz and dissolved

- HCO,

Table

to at least

date back as far as 3.8

content

2-3 permil.

but that

of this signature,

an average

(kerogen)

evolution

fractionations

system

with a minor additional

the “light” carbon

the equilibrium

- carbonate (between

(cf.

of angiosperm

overprint

matter

of perhaps

biosphere,

in fossil carbon

piled up in the Earth’s

organic

it is by no

is ample evidence

with an isotopic

do not figure prominently

the C4 pathway

achievement

on the global carbon Compared

There

of photoautotrophy

This average holds for the organic carbon kerogen

back

carbon

continuously

of sedimentary

of all ages with just minor oscillations heavy

dates

case can be built that the beginnings

Gyr ago [5,6,7,24].

reaction,

of the contemporary

1‘f a 11owance is made for a metamorphic

Gyr ago [2,21,22,23]; convincing

reservoir

to the living realm

of the key enzyme of the Calvin cycle

also on the crustal

carbon

of global carbon isotope

from the nonliving

have left their mark not only on the standing the isotopic

cycle.

FRACTIONATIONS

explanation

transfer

that the isotope-selecting organic

on the

at hand, a second look at the box model of the terrestrial

is likely to offer a straightforward

proceeds

no impact

they are confined to minor side stages of the carbon

Since the bulk of the carbon

means surprising

(I+)447

of geochemical

transformations

on Earth.

of the element

M. Schidlowski

(31448

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