The structure of the complex was refined to an R factor of 21.4% and R
free
¼ 23.6%
(for crystallographic statistics, see Supplementary Table S1). The final model includes
protein residues 25–49 and 53–148, a total of 38 RNA nucleotides, 70 water molecules and
2 sulphate ions. N-terminal residues H25 and M26 are from the vector construct. Residues
H25, D54, E80, F105, Q131 are modelled as partial side chains, whereas side chains of
residues T111, S124, L133 and Q142 exhibit double conformations. Figures were prepared
with PyMOL (http://pymol.sourceforge.net/) and GRASP
23
, and the RNA duplex
curvature was estimated using CURVES
24
.
Electrophoretic mobility shift assays
The RNA duplexes (sequences available on request) were annealed as described
6
, and
5
0
-end-labelled with
32
P. The protein–RNA binding reactions contained 100fmol RNA
duplex, 10 nmol (as monomer) full-length p19 and 5 ml 0.1 M KCl, 25 mM HEPES, 10 mM
DTT, pH 7.6. After 15 min at room temperature, 1 ml 50% glycerol and dye were added to
the reaction products and separated in a 5% polyacrylamide gel in 25 mM Tris, 192 mM
glycine, pH 8.3 at room temperature.
Received 28 September; accepted 14 November 2003; doi:10.1038/nature02213.
Published online 3 December 2003.
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Supplementary Information accompanies the paper on www.nature.com/nature.
Acknowledgements We thank members of the Patel laboratory for stimulating discussions and
A. Teplov for assistance with data collection. This research was supported by NIH. We thank the
personnel at beamline 14IDB of the Advanced Photon Source (APS) for their assistance. Use of
this APS beamline was supported by the US Department of Energy, Basic Energy Sciences, Office
of Science.
Competing interests statement The authors declare that they have no competing financial
interests.
Correspondence and requests for materials should be addressed to D.P. (pateld@mskcc.org).
Coordinates have been deposited in the Protein Data Bank under accession code 1R9F.
..............................................................
A conspicuous nickel protein
in microbial mats that
oxidize methane anaerobically
Martin Kru ¨ ger
1
, Anke Meyerdierks
1
, Frank Oliver Glo ¨ ckner
1
,
Rudolf Amann
1
, Friedrich Widdel
1
, Michael Kube
2
, Richard Reinhardt
2
,
Jo ¨ rg Kahnt
3
, Reinhard Bo ¨ cher
3
, Rudolf K. Thauer
3
& Seigo Shima
3
1
Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359 Bremen,
Germany
2
Max Planck Institute for Molecular Genetics, Ihnestraße, 14195 Berlin, Germany
3
Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Straße,
35043 Marburg, Germany
.............................................................................................................................................................................
Anaerobic oxidation of methane (AOM) in marine sediments is
an important microbial process in the global carbon cycle and in
control of greenhouse gas emission. The responsible organisms
supposedly reverse the reactions of methanogenesis
1–8
, but cul-
tures providing biochemical proof of this have not been isolated.
Here we searched for AOM-associated cell components in
microbial mats from anoxic methane seeps in the Black Sea
9–11
.
These mats catalyse AOM rather than carry out methanogenesis.
We extracted a prominent nickel compound displaying the
same absorption spectrum as the nickel cofactor F
430
of
methyl-coenzyme M reductase, the terminal enzyme of methano-
genesis
12
; however, the nickel compound exhibited a higher
molecular mass than F
430
. The apparent variant of F
430
was
part of an abundant protein that was purified from the mat
and that consists of three different subunits. Determined amino-
terminal amino acid sequences matched a gene locus cloned
from the mat. Sequence analyses revealed similarities to methyl-
coenzyme M reductase from methanogenic archaea. The abun-
dance of the nickel protein (7% of extracted proteins) in the mat
suggests an important role in AOM.
Large reservoirs of methane exceeding in mass conventional fossil
fuels lie buried in deep, sulphate-depleted marine sediments
13,14
.
Despite permanent geochemical or microbial production and
upward migration, little of the methane ever escapes into the free
ocean water. In the upper subsurface sediment, where sulphate but
no oxygen is present, most methane is scavenged by anaerobic
microbial oxidation
2,4,6,15–19
according to CH
4
þ SO
4
22
! HCO
3
2
þ
HS
2
þ H
2
O. Several in situ analyses based on isotope and lipid
signatures
5,11,13,20–22
or phylogenetic marker DNA or RNA
5,7,10,11,14,22
have suggested that the microorganisms responsible for AOM
represent special, hitherto uncultivated groups of archaea in
association with sulphate-reducing bacteria. Most of these archaea
belong to the ANME-1 and ANME-2 clusters. Both clusters are
related to the Methanosarcinales
5,7,11,14,22
. The associated, tentative
sulphate-reducing bacteria usually affiliate with the Desulfosarcina/
Desulfococcus cluster of the Deltaproteobacteria.
Besides unique microorganisms, AOM involves intriguing
mechanisms. There is still a dispute about how methane oxidation
is linked to sulphate reduction
2,6,23,24
. Furthermore, the free energy
gain from AOM (DG in situ estimated between 210 and
240 kJ mol
21
) is one of the smallest known to fuel the metabolism
of a microbial life-form
2,21,23,24
. Moreover, methane is chemically
unreactive. Mechanisms for its biochemical activation are, there-
fore, of particular interest.
A natural system that seems to be well suited for a cultivation-
independent biochemical study of AOM is microbial mats from the
cold anoxic methane seeps of the northwestern Black Sea shelf
9–11
.
These mats provide sufficient biomass to record a cytochrome
spectrum
9
. They harbour archaea of the ANME-1 cluster that
account for up to 70% of the cells detectable in situ
11
. Cells of the
letters to nature
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