In PNAS, Wing and Halevy (1) present a new model that quantitatively describes the magnitude of sulfur isotope fractionation produced by dissimilatory microbial sulfate reduction (MSR). MSR is a major player in the global biogeochemical cycles and is responsible for the respiration of up to 30% of organic matter in marine sediments (2). This metabolism produces large isotope effects, in which the product, sulfide, is depleted in the heavy isotopes (^(33)S, ^(34)S, and ^(36)S) relative to the most abundant isotope ^(32)S (3), enriching modern seawater sulfate in ^(34)S by about 21‰ (parts per thousand) compared with mantle sulfur. Sedimentary sulfur minerals preserve a record of this effect and are used to track changes in the sulfur isotope composition of seawater and the biogeochemical sulfur, carbon, and oxygen cycles through geologic time (4). Such reconstructions require an understanding of factors that control the magnitude of sulfur isotope effects and dictate the fractionation of sulfur isotopes by sulfate reducers under a range of growth conditions

Bosak, Tanja

Ono, Shuhei

Sim, Min Sub

PubMed

In PNAS, Wing and Halevy present a new model that quantitatively describes the magnitude of sulfur isotope fractionation produced by dissimilatory microbial sulfate reduction (MSR). MSR is a major player in the global biogeochemical cycles and is responsible for the respiration of up to 30% of organic matter in marine sediments. This metabolism produces large isotope effects, in which the product, sulfide, is depleted in the heavy isotopes ([superscript 33]S, [superscript 34]S, and [superscript 36]S) relative to the most abundant isotope [superscript 32]S (3), enriching modern seawater sulfate in [superscript 34]S by about 21‰ (parts per thousand) compared with mantle sulfur. Sedimentary sulfur minerals preserve a record of this effect and are used to track changes in the sulfur isotope composition of seawater and the biogeochemical sulfur, carbon, and oxygen cycles through geologic time (4). Such reconstructions require an understanding of factors that control the magnitude of sulfur isotope effects and dictate the fractionation of sulfur isotopes by sulfate reducers under a range of growth conditions

DSpace@MIT

Proceedings of the National Academy of Sciences

Predictive isotope model connects microbes in culture and nature

Caltech Authors - Main

COMMENTARY
Predictive isotope model connects microbes
in culture and nature
Shuhei Onoa,1, Min Sub Simb, and Tanja Bosaka
aDepartment of Earth, Atmospheric, and Planetary Sciences, Massachusetts Institute of
Technology, Cambridge, MA 02139; and bDivision of Geological and Planetary Sciences,
California Institute of Technology, Pasadena, CA 91125
In PNAS, Wing and Halevy (1) present a new
model that quantitatively describes the mag-
nitude of sulfur isotope fractionation pro-
duced by dissimilatory microbial sulfate
reduction (MSR). MSR is a major player in
the global biogeochemical cycles and is re-
sponsible for the respiration of up to 30%
of organic matter in marine sediments (2).
This metabolism produces large isotope
effects, in which the product, sulfide, is de-
pleted in the heavy isotopes (33S, 34S, and 36S)
relative to the most abundant isotope 32S (3),
enriching modern seawater sulfate in 34S by
about 21‰ (parts per thousand) compared
with mantle sulfur. Sedimentary sulfur min-
erals preserve a record of this effect and are
used to track changes in the sulfur isotope
composition of seawater and the biogeo-
chemical sulfur, carbon, and oxygen cycles
through geologic time (4). Such reconstruc-
tions require an understanding of factors
that control the magnitude of sulfur isotope
effects and dictate the fractionation of sulfur
isotopes by sulfate reducers under a range of
growth conditions.
All models of sulfur isotope fractionation
during MSR, including that of Wing and
Halevy (1), attempt to describe the interpre-
tations of sulfur isotope signals produced in
inherently complex natural systems and for-
malize trends bolstered by decades of obser-
vations and laboratory studies. Some of the
most prominent trends show that: (i) the
fractionation of S isotopes correlates inversely
with the cell-specific sulfate reduction rates
(csSRR) (Fig. 1), implying that the sluggish
flow of electrons toward the sulfate-reducing
pathway increases the magnitude of isotope
fractionation (34e) (3, 5–8); (ii) the magnitude
of isotope fractionation depends on the actual
electron transfer pathway and organism (Fig.
1) (9); and (iii) low fractionations are likely in
sulfate-limited environments (10, 11).
The new model by Wing and Halevy (1)
relies on these observations and interprets
some of the model parameters in the light
of organismal biochemistry to get around
the microbe- or pathway-specific effects.
Conceptual origins of this work date back to
the model put forward by Rees (12) in the
early 1970s. Rees’ model (12) explained the
net observed sulfur isotope fractionations by
considering the following biochemical steps
involved in MSR: activation of sulfate as
adenosine-5′-phosphosulfate (APS), reduc-
tion of APS to sulfite, and further reduction
of sulfite to sulfide. The model assigned in-
trinsic isotope fractionation factors for the
two reduction steps and for the sulfate up-
take, as do Wing and Halevy (1), and ex-
plored the range of reversibilities at each
step. A later study by Farquhar et al. (13)
added triple sulfur isotope systematics
(32S/33S/34S), whereas Brunner and Bernas-
coni (14) updated the fractionation factors
to explain large (>50‰) sulfur isotope frac-
tionations observed in nature. These models
could explain the range of sulfur isotope frac-
tionations seen in nature, but their output
was not related to environmental parameters,
such as the concentrations of sulfate and sul-
fide, limiting the predictive power. Experi-
mental tests of the assumptions made by
these models have also proven difficult.
The Wing and Halevy model (1) is the
first to explicitly interpret some of its free
parameters using thermodynamics and the
influence of electron transfer to the sul-
fate-reducing pathway. The reversibility is
elegantly related to the free energy of reactions
and processes (also see ref. 15). The estimated
free energy of the reactions under standard
conditions (ΔG0) then allows the reversibility
to be quantified as a function of activities of
products and reactants. With reasonable
assumptions (e.g., fast equilibrium for H2S
inside and outside of the cell), the new model
predicts the net fractionation from only three
assumed parameters: (i) sulfur isotope effect
during the uptake of sulfate (other fraction-
ation factors are fixed), (ii) overall redox po-
tential of the cell, described as the ratios of
oxidized and reduced forms of menaquinone,
and (iii) a scaling factor, interpreted as the
ratio of in vivo enzyme activities to those
measured in in vitro crude cell extracts. One
of the main contributions of this model will
be to inspire future experimental tests of these
generalizations.
The Wing and Halevy model (1) uses the
results of recent culture studies (5, 6, 8, 13)
and produces some new, experimentally test-
able predictions and observations. As men-
tioned earlier, experimental studies show
a tight correlation between 34e and cell-spe-
cific sulfur reduction rate (csSRR), but the
exact relationship differs from one model mi-
crobe to another (Fig. 1). Wing and Halevy
Fig. 1. Relationship between cell specific sulfate reduc-
tion rates, growth rates, and isotope fractionation factors
for three different strains of sulfate-reducing bacteria. Data
from refs. 5–8.
Author contributions: S.O., M.S.S., and T.B. wrote the paper.
The authors declare no conflict of interest.
See companion article on page 18116.
1To whom correspondence should be addressed. Email: sono@mit.
edu.
18102–18103 | PNAS | December 23, 2014 | vol. 111 | no. 51 www.pnas.org/cgi/doi/10.1073/pnas.1420670111
(1) attribute this difference to species-specific
properties: for example, differences in the
activities and abundances of respiratory
enzymes, with higher abundances expected
at higher growth rates (1). The authors pro-
pose proteomic tests for these predictions.
Proteomic studies of sulfate reducers are
few, but a study by Zhang et al. (16) showed
the same abundance of dissimilatory sulfite
reductase (Dsr) in cultures of Desulfovibrio
vulgaris grown on lactate and formate, de-
spite different growth rates. This discrep-
ancy encourages future proteomic analyses
of samples from continuous cultures and
measurements of Dsr abundances as a func-
tion of csSRR, rather than growth rate.
Assumptions about enzyme abundances,
activities, csSRRs, and growth rates intrinsic
to different microbes can also be investi-
gated by mutagenesis experiments, com-
parative genomics, measurements of the
isotopic composition of intracellular inor-
ganic sulfur species, and simple biochemical
assays that target the abundances of specific
redox-active components, such as ferredoxin,
NADH/NAD+, and cytochromes, all recog-
nized players in the electron transfer toward
the sulfate-reducing pathway of different
sulfate-reducing bacteria (9, 17).
The new model by Wing and Halevy (1) is
also used to clarify the relationship between
the magnitude of isotope fractionation and
environmental sulfate levels, a key question
related to the cycling of sulfur on early Earth.
Because S isotope fractionations in the rocks
of Archean age (>2.5 billion years ago) are
typically small, low micromolar levels of sea-
water sulfate were assumed (10, 11), although
alternative explanations also existed (18).
Wing and Halevy (1) suggest that fractiona-
tions as large as 60–70‰ are possible in the
presence of micromolar sulfate, as long as
sluggish net respiration rates can be main-
tained. This theory is consistent with a recent
report of high fractionations from a low sul-
fate environment (10), but experimental ver-
ification of the model assumptions will be
truly challenging.
Wing and Halevy (1) predict that D. vul-
garis reducing much less than 1 fmol of
sulfate per cell per day should produce
34e of 60‰. For DMSS-1, a recent ma-
rine isolate different from D. vulgaris, the
The Wing and Halevy
model is the first to
explicitly interpret some
of its free parameters
using thermodynamics
and the influence of
electron transfer to
the sulfate-reducing
pathway.
predicted rate (csSRR) is smaller than
0.5 fmol sulfate per cell per day irrespective
of sulfate level (figure 3 in ref. 1). Note that
much slower csSSRs, from 0.1 to 0.0001 fmol
per cell per day (19), are observed in nature.
In lactate-grown cultures, 0.5 fmol per cell
per day roughly corresponds to the growth
rate of 0.05 per day (Fig. 1). In continuous
cultures, this growth rate translates to the
turnover time of 20 days, and three-times
longer experiments are ideal to ensure
a complete reservoir exchange, which is
possible but not trivial. Furthermore, the
maintenance energy requirements may set
the low limit on the respiration rate attain-
able in chemostat experiments, such that
csSRRs much smaller than 0.5 fmol sulfate
per cell per day may not be attainable (20).
The use of high-energy electron donors, such
as glucose (5), may be one way to circumvent
the issue of maintenance energy, although
such donors are not commonly explored in
experimental studies. Therefore, a funda-
mental value of models, including the one by
Wing and Halevy (1), is the ability to make
predictions under environmental conditions
that elude culture experiments (10, 19).
Microbial sulfate reduction connects ecol-
ogy, biochemistry, geochemistry, physiology,
and Earth history. The predictive power of
the model byWing andHalevy (1) improves
our quantitative understanding of these
links and provides a new tool with which
to explore the evolution of the sulfur cycle
from billions of years ago to today.
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Ono et al. PNAS | December 23, 2014 | vol. 111 | no. 51 | 18103
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Predictive isotope model connects microbes in culture and nature

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