8
Sulfur Cycling and Methane Oxidation
282
The first step in this reaction (Eq. 8.9) is
obviously a reversal of methanogenesis from CO 2
and H 2 shown in Eq. 8.7. How can a metabolic
process run in two opposite directions and yet
yield energy for both types of archaea? Hoehler
et al. (1994, 1998) showed that the energy yield is
highly dependent on the H 2 concentration which,
in turn, is regulated by the predominant process
of mineralization. In the deep methanogenic zone
the H 2 concentration is relatively high, about 10
nM, so that methanogenesis (Eq. 8.7) is an exergonic, energy yielding process. In the sulfate
zone, the sulfate reducing bacteria maintain such a
low H 2 concentration, about, 1 nM, that it falls
below the concentration required for an exergonic
methanogenesis. On the contrary, the reversal of
methanogenesis (Eq. 8.9) becomes exergonic and
AOM may proceed. This strong dependence on
H 2 concentration could explain why the methane
oxidizing archaea grow in aggregates together
with the sulfate reducing bacteria. Only when the
sulfate reducers efficiently scavenge H 2 as it is
produced by the archaea are these able to continue oxidizing methane.
Although this idea of a syntrophic association
based on inter-species hydrogen transfer is very
appealing, it explains only a part of the observations on AOM. Since both the methanotrophic
archaea and the sulfate reducing bacteria carry the
light carbon isotopic signal of methane, it is a
question how also carbon is transferred in this
syntrophic association. An alternative pathway
could therefore be the conversion of methane to
acetate and the subsequent oxidation of acetate
(CH 3 COO
-
) by the sulfate reducers with a concurrent incorporation of part of the acetate into
their cell biomass:
CH 4 + HCO 3
-
→ CH 3 COO
-
+ H 2 O
(8.11)
SO 4
2+ CH 3 COO
-
→ HS
-
+ 2 HCO 3
-
(8.12)
Further possibilities exist, such as a combined
transfer of acetate and hydrogen or a transfer of
formate, both of which may explain the δ
13
C observations and be more compatible with the energetic
constraints on AOM (Valentine and Reeburgh
2000; Sørensen et al. 2001). Further research is
required to understand the basic mechanism and
regulation of this key process in the methane
cycle.
Although AOM provides an almost complete
barrier to methane escape from the sea floor in
sediments with diffusive methane flux, the process
is surprisingly sluggish and takes place over a
sediment horizon and a time scale that highly
exceed that of most other microbial processes in
gradient environments. Thus, the life-time of
methane upon diffusion up into the sulfate zone is
generally on the order of months to years
(Jørgensen et al. 2004). This is a reason why we
prefer the term “sulfate-methane transition” rather
than “sulfate-methane interface”. A reason for the
slow turnover may be that the methane oxidizing
community is operating near the theoretical minimum in energy yield required for microbial growth.
The estimated energy yield of AOM in a number
of sedimentary environments is -20 to -25 kJ per
mol of methane consumed (Hoehler et al. 1994)
which is less than the energy required for the
formation of ATP (see Chapter 5). If the process
does indeed involve a two-step reaction such as
suggested in Eq. 8.9-8.10 or 8.11-8.12, then this
energy even has to be shared among two partners.
This may explain why the growth of AOM aggregates is exceedingly slow and requires many
months for a doubling of the biomass in laboratory incubations (Nauhaus et al. 2002). It may also
explain why anaerobic methane oxidizing microorganisms have not yet been isolated in pure
culture in the laboratory. They simply grow so
slow that isolation may take many years. These
observations demonstrate, however, that processes catalyzed by microbial communities in the
environment can be highly efficient in energy
conservation and operate close to the theoretical
thermodynamic limits (Schink 1997; Hoehler et al.
2001; Jackson and McInerney 2002).
By the use of molecular methods based on
sequence information from 16S rRNA genes, a
broad diversity of archaea that all belong to the
Euryarchaeota (Orphan et al. 2002; Knittel et al.
2005) and sulfate reducing bacteria mostly
belonging to the Desulfosarcina-Desulfococcus
branch of the Delta-proteobacteria (Boetius et al.
2000; Orphan et al. 2001) has been consistently
found to be associated with anaerobic oxidation
of methane. Although the genetic identity of AOM
microorganisms is now revealed, the physiology
and biochemistry of AOM are still incompletely
understood. A recent clue came from the discovery that the terminal key enzyme of methanogenesis, methyl coenzyme M reductase, and its
encoding gene seem also to be involved in the
process of AOM in a slightly modified form, thus
indicating that AOM may partly be a reversal of
Sulfur Cycling and Methane Oxidation
282
The first step in this reaction (Eq. 8.9) is
obviously a reversal of methanogenesis from CO 2
and H 2 shown in Eq. 8.7. How can a metabolic
process run in two opposite directions and yet
yield energy for both types of archaea? Hoehler
et al. (1994, 1998) showed that the energy yield is
highly dependent on the H 2 concentration which,
in turn, is regulated by the predominant process
of mineralization. In the deep methanogenic zone
the H 2 concentration is relatively high, about 10
nM, so that methanogenesis (Eq. 8.7) is an exergonic, energy yielding process. In the sulfate
zone, the sulfate reducing bacteria maintain such a
low H 2 concentration, about, 1 nM, that it falls
below the concentration required for an exergonic
methanogenesis. On the contrary, the reversal of
methanogenesis (Eq. 8.9) becomes exergonic and
AOM may proceed. This strong dependence on
H 2 concentration could explain why the methane
oxidizing archaea grow in aggregates together
with the sulfate reducing bacteria. Only when the
sulfate reducers efficiently scavenge H 2 as it is
produced by the archaea are these able to continue oxidizing methane.
Although this idea of a syntrophic association
based on inter-species hydrogen transfer is very
appealing, it explains only a part of the observations on AOM. Since both the methanotrophic
archaea and the sulfate reducing bacteria carry the
light carbon isotopic signal of methane, it is a
question how also carbon is transferred in this
syntrophic association. An alternative pathway
could therefore be the conversion of methane to
acetate and the subsequent oxidation of acetate
(CH 3 COO
-
) by the sulfate reducers with a concurrent incorporation of part of the acetate into
their cell biomass:
CH 4 + HCO 3
-
→ CH 3 COO
-
+ H 2 O
(8.11)
SO 4
2+ CH 3 COO
-
→ HS
-
+ 2 HCO 3
-
(8.12)
Further possibilities exist, such as a combined
transfer of acetate and hydrogen or a transfer of
formate, both of which may explain the δ
13
C observations and be more compatible with the energetic
constraints on AOM (Valentine and Reeburgh
2000; Sørensen et al. 2001). Further research is
required to understand the basic mechanism and
regulation of this key process in the methane
cycle.
Although AOM provides an almost complete
barrier to methane escape from the sea floor in
sediments with diffusive methane flux, the process
is surprisingly sluggish and takes place over a
sediment horizon and a time scale that highly
exceed that of most other microbial processes in
gradient environments. Thus, the life-time of
methane upon diffusion up into the sulfate zone is
generally on the order of months to years
(Jørgensen et al. 2004). This is a reason why we
prefer the term “sulfate-methane transition” rather
than “sulfate-methane interface”. A reason for the
slow turnover may be that the methane oxidizing
community is operating near the theoretical minimum in energy yield required for microbial growth.
The estimated energy yield of AOM in a number
of sedimentary environments is -20 to -25 kJ per
mol of methane consumed (Hoehler et al. 1994)
which is less than the energy required for the
formation of ATP (see Chapter 5). If the process
does indeed involve a two-step reaction such as
suggested in Eq. 8.9-8.10 or 8.11-8.12, then this
energy even has to be shared among two partners.
This may explain why the growth of AOM aggregates is exceedingly slow and requires many
months for a doubling of the biomass in laboratory incubations (Nauhaus et al. 2002). It may also
explain why anaerobic methane oxidizing microorganisms have not yet been isolated in pure
culture in the laboratory. They simply grow so
slow that isolation may take many years. These
observations demonstrate, however, that processes catalyzed by microbial communities in the
environment can be highly efficient in energy
conservation and operate close to the theoretical
thermodynamic limits (Schink 1997; Hoehler et al.
2001; Jackson and McInerney 2002).
By the use of molecular methods based on
sequence information from 16S rRNA genes, a
broad diversity of archaea that all belong to the
Euryarchaeota (Orphan et al. 2002; Knittel et al.
2005) and sulfate reducing bacteria mostly
belonging to the Desulfosarcina-Desulfococcus
branch of the Delta-proteobacteria (Boetius et al.
2000; Orphan et al. 2001) has been consistently
found to be associated with anaerobic oxidation
of methane. Although the genetic identity of AOM
microorganisms is now revealed, the physiology
and biochemistry of AOM are still incompletely
understood. A recent clue came from the discovery that the terminal key enzyme of methanogenesis, methyl coenzyme M reductase, and its
encoding gene seem also to be involved in the
process of AOM in a slightly modified form, thus
indicating that AOM may partly be a reversal of