Download Carbon cycle: New pathways in the sand

news & views
CARBON CYCLE
New pathways in the sand
Organic carbon decomposition in anoxic marine sediments was thought to be dominated by bacteria, but
experimental data and microbial culture studies now show that microalgae buried in coastal sands may also play an
important role in carbon turnover.
Alexandra Rao
T
he shallow ocean margins occupy
only a small fraction of the surface
area of the world ocean, but they
support highly productive ecosystems that
play a disproportionate role in the marine
carbon cycle1. Much of the biomass that
sinks out of the sunlit ‘euphotic’ surface
ocean is oxidized or ‘remineralized’,
producing CO2 and nutrients in the
shallow seafloor. On the margins, the
seafloor is dominated by coarse sand and
gravel2. These permeable sediments act as
efficient bioreactors — the rapid flushing
of bottom water oxidants and particulate
organic material into these deposits fuels
high rates of remineralization by sediment
microbial communities3. Until now, this
process was believed to be driven mainly
by bacteria and archaea4. Writing in Nature
Geoscience, Bourke et al.5 show that another
group of microorganisms — eukaryotic
microalgae — may be responsible
for organic matter decomposition in
permeable sediments. They found that dark
fermentation by diatoms and green algae
was responsible for CO2 and molecular H2
production in anoxic coastal sands.
Organic matter remineralization at
the seafloor proceeds by the sequential
reduction of available oxidants in order of
decreasing energy yield — oxygen, nitrate,
manganese and iron oxides, sulfate —
followed by methane production6. This
‘diagenetic sequence’ of reduction–
oxidation reactions — together considered
to be one of the pillars of marine
biogeochemistry — agrees well with
observations in fine, cohesive sediments. In
this classical paradigm, the remineralization
of organic matter is mainly mediated
by bacteria and archaea: prokaryotic
unicellular microorganisms that display
a great diversity of metabolic strategies.
Eukaryotes, in contrast, are structurally
more complex organisms whose energy
generation strategies rely on aerobic or
fermentative pathways of organic carbon
decomposition. There has been growing
recognition of the importance of benthic
photosynthesis by unicellular eukaryotic
Oxic
Photosynthesis
O2
H2O
NO3–
N2
Mn4+
Mn2+
Ripple migration
and resuspension
Fe3+
Fe2+
SO42–
H2S
Fermentation
CO2 + H2
Anoxic
Hydrogenotrophic
bacteria
CO2
CH4, CH3COOH
U(vi)
U(iv)
Figure 1 | The role of microalgae in energy transfer in coastal sands. Microalgae carry out photosynthesis
in surface sands but are often buried below the oxic layer where they can persist by fermenting
intracellular organic compounds, as shown by Bourke and colleagues5. H2 produced by this process is a
valuable energy source and might fuel the growth of hydrogenotrophic bacteria in sediments, oxidizing
H2 with a variety of electron acceptors. This secondary microbial production is available to be grazed by
sediment-dwelling fauna.
microalgae in surface sands within the
euphotic zone3,7. We now know that diatoms
can survive in dark, anoxic conditions using
alternative metabolic strategies such as the
dissimilatory reduction of intracellular
nitrate to ammonium8. In anaerobic
conditions, some algae can also carry out
fermentation9 — generating energy in the
absence of external oxidants by transferring
electrons between organic compounds,
that is, oxidizing some carbon atoms in
the substrate while reducing others. These
discoveries were based on laboratory
culture experiments, but they hinted at the
long-term survival of microalgae buried
in sediments.
Bourke et al.5 used flow-through reactor
experiments to quantify the importance
of different pathways of organic carbon
remineralization in anoxic coastal sands
from Australia and Denmark. They found
that methanogenesis and the reduction of
nitrate, iron and sulfate could not account
for the rate of CO2 production by anoxic
remineralization in the reactor sands.
Bourke and colleagues also discovered that
CO2 production was not affected by the
addition of a broad spectrum antibiotic, but
it did cease after the addition of mercuric
chloride — a more general biocide. These
experiments point to a eukaryotic metabolic
pathway. Intriguingly, CO2 production in
anoxic reactor sediments was accompanied
by the release of gaseous H2, which was
similarly unaffected by an antibiotic
treatment, but blocked by the inhibition of
a hydrogenase enzyme that is required for
dark fermentation. H2 is produced in some
microbial nitrogen fixation and fermentation
pathways by the enzymes nitrogenase and
hydrogenase, as a way to release excess
reductant10. This source of energy can
NATURE GEOSCIENCE | ADVANCE ONLINE PUBLICATION | www.nature.com/naturegeoscience
1
.
d
e
v
r
e
s
e
r
s
t
h
g
i
r
l
l
A
.
e
r
u
t
a
N
r
e
g
n
i
r
p
S
f
o
t
r
a
p
,
d
e
t
i
m
i
L
s
r
e
h
s
i
l
b
u
P
n
a
l
l
i
m
c
a
M
6
1
0
2
©
news & views
then fuel microbial aerobic and anaerobic
hydrogen oxidation, also mediated by
hydrogenase enzymes.
This clever bit of detective work provides
compelling evidence that H2 and CO2
production in anoxic reactor sands was
driven by eukaryotic fermentation. To
substantiate this argument, Bourke et al.5
looked for the release of fermentation
products. They found an accumulation of
lipids in reactor sediments, consistent with
intracellular storage previously observed
in green algae. Cultures of diatoms and
green algae isolated from the two study
sites produced H2 in anoxic incubations,
further confirming the observation of
microalgal dark fermentation in the
reactor experiments.
These results raise important questions
concerning the fate of H2 released by
eukaryotic fermentation in coastal sands.
Many hydrogenotrophic bacteria obtain
energy by oxidizing H2 with various
electron acceptors such as oxygen, nitrite,
nitrate, iron(III), manganese(IV), different
sulfur compounds and uranium(VI)
2
(Fig. 1)10. If H2 is produced by eukaryotic
fermentation, then the growth of
hydrogenotrophic bacteria that might stem
from this energy source represents a form
of secondary production, and it probably
plays a significant ecological role in the
transfer of energy from organic matter
decomposition by the sediment microbial
community. The search is now on to
examine the effect of these pathways on
biogeochemistry and microbial ecology in
permeable sediments.
Bourke and colleagues5 present the
first evidence that eukaryotes play an
important role in the remineralization of
organic carbon in marine sands. But how
important is this pathway in the turnover
of carbon on continental shelves? About
70% of the global shelf area is covered by
coarse sands2, in which fluid advection
can flush microalgal biomass to 15 cm
depth3. The relative importance of aerobic
and anaerobic metabolic pathways in
permeable sediments are poorly constrained.
Yet, if oxygen penetrates to 5 cm depth
in sandy sediments11 and eukaryotic
dark fermentation accounts for 90% of
organic carbon remineralization in anoxic
conditions, then this mechanism may
account for up to 40% of carbon turnover on
the continental shelf. If so, then a substantial
revision of our understanding of elemental
cycling in ocean margins is in order.
❐
Alexandra Rao is at the Institut des sciences de la
mer de Rimouski, Université du Québec à Rimouski,
310 allée des Ursulines, Rimouski, Québec
G5L 3A1, Canada.
e-mail: [email protected]
References
Walsh, J. J. Nature 350, 53–55 (1991).
Emery, K. O. Am. Assoc. Petrol. Geol. Bull. 52, 445–464 (1968).
Huettel, M. et al. Ann. Rev. Mar. Sci. 6, 23–51 (2014).
Nealson, K. H. Annu. Rev. Earth Planet. Sci. 25, 403–434 (1997).
Bourke, M. F. et al. Nat. Geosci. http://dx.doi.org/10.1038/
ngeo2843 (2016).
6. Froelich, P. et al. Geochim. Cosmochim. Acta 43, 1075–1090 (1979).
7. Jahnke, R. A. et al. Cont. Shelf Res. 20, 109–127 (2000).
8. Kamp, A. et al. Proc. Natl Acad. Sci. USA 108, 5649–5654 (2011).
9. Atteia, A. et al. Biochim. Biophys. Acta 1827, 210–223 (2013).
10.Schwartz, E. & Friedrich, B. Prokaryotes 2, 496–563 (2006).
11.Reimers, C. E. et al. Cont. Shelf Res. 24, 183–201 (2004).
1.
2.
3.
4.
5.
Published online: 28 November 2016
NATURE GEOSCIENCE | ADVANCE ONLINE PUBLICATION | www.nature.com/naturegeoscience
.
d
e
v
r
e
s
e
r
s
t
h
g
i
r
l
l
A
.
e
r
u
t
a
N
r
e
g
n
i
r
p
S
f
o
t
r
a
p
,
d
e
t
i
m
i
L
s
r
e
h
s
i
l
b
u
P
n
a
l
l
i
m
c
a
M
6
1
0
2
©