Community Size and Metabolic Rates of Psychrophilic Sulfate-Reducing Bacteria in Arctic Marine Sediments

Abstract

The numbers of sulfate reducers in two Arctic sediments with in situ temperatures of 2.6 and -1.7 degrees C were determined. Most-probable-number counts were higher at 10 degrees C than at 20 degrees C, indicating the predominance of a psychrophilic community. Mean specific sulfate reduction rates of 19 isolated psychrophiles were compared to corresponding rates of 9 marine, mesophilic sulfate-reducing bacteria. The results indicate that, as a physiological adaptation to the permanently cold Arctic environment, psychrophilic sulfate reducers have considerably higher specific metabolic rates than their mesophilic counterparts at similarly low temperatures.

Full text

APPLIED AND ENVIRONMENTAL MICROBIOLOGY,
0099-2240/99/$04.00⫹0
Sept. 1999, p. 4230–4233 Vol. 65, No. 9
Copyright © 1999, American Society for Microbiology. All Rights Reserved.
Community Size and Metabolic Rates of Psychrophilic Sulfate-
Reducing Bacteria in Arctic Marine Sediments
CHRISTIAN KNOBLAUCH,
1
* BO BARKER JØRGENSEN,
1
AND JENS HARDER
2
Departments of Biogeochemistry
1
and Microbiology,
2
Max Planck Institute for
Marine Microbiology, D-28359 Bremen, Germany
Received 11 March 1999/Accepted 2 July 1999
The numbers of sulfate reducers in two Arctic sediments with in situ temperatures of 2.6 and ⴚ1.7°C were
determined. Most-probable-number counts were higher at 10°C than at 20°C, indicating the predominance of
a psychrophilic community. Mean specific sulfate reduction rates of 19 isolated psychrophiles were compared
to corresponding rates of 9 marine, mesophilic sulfate-reducing bacteria. The results indicate that, as a phys-
iological adaptation to the permanently cold Arctic environment, psychrophilic sulfate reducers have consid-
erably higher specific metabolic rates than their mesophilic counterparts at similarly low temperatures.
Dissimilatory sulfate reduction is the most important bacte-
rial process in anoxic marine sediments, accounting for up to
half of the total organic carbon remineralization (4, 12, 21).
Since more than 90% of the global sea floor is cold (⬍4°C
[19]), sulfate reducers must be able to metabolize and grow at
low ambient temperatures. Sulfate reduction rates (SRRs) in
polar sediments may be similar to those of temperate environ-
ments (14, 21, 24, 28), but sulfate reducers active in polar
sediments have not been isolated and studied.
Similar SRRs in cold and temperate sediments could be
explained either by (i) the presence of more sulfate reducers in
cold environments, thus compensating for lower per-cell SRRs
(i.e., cell-specific SRRs) at low temperatures, or by (ii) com-
parable community sizes in both environments but higher
specific respiration rates of psychrophiles relative to those of
mesophiles at low temperatures. In the present study, both
possibilities were investigated by quantifying sulfate reducers
in two polar sediments as well as by comparing specific SRRs
of new psychrophilic isolates to those of known mesophilic
sulfate-reducing bacteria (SRB). Because the phylogeny and
physiology of sulfate reducers living in polar sediments were
previously unknown, we used the most-probable-number
(MPN) method to count and subsequently isolate the most
abundant cultivable sulfate reducers for further pure-culture
studies.
Two permanently cold sediments, located off the coast of
Svalbard, Hornsund (76°58⬘2⬙N, 15°34⬘5⬙E; in situ tempera-
ture, 2.6°C) and Storfjord (77°33⬘0⬙N, 19°05⬘0⬙E; in situ tem-
perature, ⫺1.7°C), were sampled during a cruise in September
and October of 1995. For further information about sampling
sites, see Kostka et al. (18). Sediment was collected with a
multicorer, and one individual core (referred to as core A) was
subsampled for enumeration of sulfate reducers by triplicate
MPN series (2), SRR measurements by the whole-core method
(11), and nucleic acid analysis (25). The subcores were sliced
on the ship, and samples from five sediment layers between the
surface and 30-cm depth (Fig. 1) were transferred to liquid
medium (17) containing either lactate (20 mM) or acetate (15
mM). Additionally, single-dilution series with propionate (20
mM) or propanol (20 mM) were inoculated. The cultures were
incubated at 4, 10, and 20°C in our laboratory, and growth of
sulfate reducers was monitored by measuring sulfide produc-
tion during the following 30 months.
At both sampling sites, the maximum MPN counts of SRB
occurred in the top 6 cm of the sediment. In particular in
Storfjord, the highest SRRs occurred at a deeper layer than the
maximum cell counts (Fig. 1). Below that depth, cell numbers
decreased sharply. Maximum cell numbers were generally de-
tected in MPN series incubated at 10°C with lactate as the
substrate (Fig. 1b and d). Higher cell numbers at 10°C than at
20°C indicate that the majority of cultivable sulfate reducers in
the sediment are unable to grow at 20°C, thus providing the
first microbiological evidence for a predominantly psychro-
philic sulfate reducer community in a marine sediment. Max-
imum MPNs with acetate as the substrate were 10- to 100-fold
lower than those with lactate as the substrate for cultures and
were always highest at 20°C. These results are probably due to
extremely slow growth of acetate oxidizers at 4 and 10°C and
not to a mesophilic acetate-oxidizing SRB community. This
conclusion is supported by the facts that the first positive en-
richments of samples collected at Storfjord, incubated at 4 and
10°C on acetate, were detected after more than 6 months and
that counts increased slowly during the following 2 years.
In contrast to this microbiological evidence for a community
with a psychrophilic growth potential (optimum temperature,
below 20°C), Sagemann et al. (24) measured the highest SRRs
for Hornsund and Storfjord sediments at 27°C. These process
rate measurements seem to contradict our results from MPN
counts. However, Isaksen and Jørgensen (9) demonstrated that
a moderately psychrophilic SRB had an optimum temperature
for sulfate reduction (28°C) 10°C higher than that for growth
(18°C). This result indicates that the observed maximum SRRs
at 27°C in the Svalbard sediments might still be assigned to a
psychrophilic community.
MPN counts yielded no evidence for a larger community size
of cultivable sulfate reducers in Arctic sediments relative to
temperate sediments since maximum cell counts, e.g. 4.3 ⫻ 10
5
cells cm
⫺3
for Hornsund sediments (Fig. 1b), are in the range
of those reported previously for temperate marine sediments
(2 ⫻ 10
5
to 2 ⫻ 10
6
cells cm
⫺3
(13, 20, 27). Furthermore,
parallel slot blot hybridizations indicate that numbers of SRB
in Hornsund and Storfjord are comparable to those in temper-
ate sediments (25, 26). If the community size and the SRRs in
Arctic and temperate habitats are similar, then SRRs per cell
* Corresponding author. Mailing address: Max Planck Institute for
Marine Microbiology, Celsiusstr. 1, D-28359 Bremen, Germany. Phone:
49 421 2028 653. Fax: 49 421 2028 690. E-mail: cknoblau@mpi-bremen
.de.
4230

must be comparable too, irrespective of the temperature dif-
ference.
To test this possibility, pure cultures of Arctic SRB were
isolated from the highest dilution steps of the MPN enrich-
ments by the modified deep-agar dilution technique (10). At
20°C, only three pure cultures could be isolated because most
enrichments did not continue to grow after a transfer to fresh
medium. None of these isolates is able to grow at the in situ
temperature of the sampling sites, providing further evidence
that the community active in the sediments is psychrophilic. At
4 and 10°C, 30 different strains were isolated from the MPN
enrichments. Based on a preliminary physiological and phylo-
genetic characterization, 19 psychrophilic strains were selected
for further studies. All strains except LSv22 had optimum
temperatures below 20°C, and only three isolates grew at 26°C
(Table 1). More relevant, however, is that they are the first
isolates that grow at a typical temperature for polar sediments,
i.e., the freezing point of seawater, ⫺1.8°C (Table 1). Doubling
times at ⫺1.8°C were 4 to 6 days for the lactate-grown strains
LSv54, LSv514 and LSv21 but more than 5 weeks for the
acetate- and propionate-grown strains ASv26 and PSv29 (16).
To compare SRRs of psychrophiles and mesophiles at the
temperatures of their respective habitats, the specific SRRs of
psychrophilic SRB were measured at the in situ temperatures
of the Arctic sediments (2.6 and ⫺1.7°C) and SRRs for 9
mesophiles were measured at 4, 8, and 13°C, temperatures in
the range normally encountered in temperate sediments. All
cultures were grown to the exponential growth phase, and rates
were measured with the radiotracer method as described else-
where (16). Specific SRRs of psychrophiles at 2.6 and ⫺1.7°C
varied between 1 and 42 fmol cell
⫺1
day
⫺1
(Table 1). All
mesophiles reduced sulfate at 4°C, although only Desulfobacter
hydrogenophilus was able to grow at that temperature. Specific
SRRs of all mesophiles except D. hydrogenophilus (Table 2)
increased exponentially with increasing temperatures but were
still comparable to those found for the psychrophiles at tem-
peratures 6 to 10°C lower. Since it is difficult to directly com-
pare rates for mesophiles and psychrophiles at low tempera-
tures because their growth temperature ranges do not overlap,
we fitted mean rates for mesophiles by the Arrhenius equation:
rate ⫽ A 䡠 exp(⫺E
a
䡠 [R 䡠 T]
⫺1
), where A is a constant, E
a
is
apparent activation energy, R is the gas constant, and T is
absolute temperature expressed in Kelvins. The fit was extrap-
olated to ⬍0°C and compared to rates for psychrophiles (Fig.
2). Calculated rates for mesophiles at 2.6 and ⫺1.7°C were
three- to fourfold lower than the measured rates for psychro-
philes at the same temperatures (Fig. 2). The comparison of
biomass-specific SRRs yielded similar differences (data not
FIG. 1. Depth profile of SRRs in Hornsund (a) and Storfjord (c) at in situ temperatures and MPN counts of SRB in Hornsund (b) and Storfjord (d) sediments.
MPN series were incubated at different temperatures with either lactate (
^
, 20°C;
o
, 10°C;
_
, 4°C) or acetate (
䊐
, 20°C;
p
, 10°C;
䡺
, 4°C). Horizontal bars represent 95% confidence intervals, and vertical bars indicate the depths of sediments used for MPN enrichments.
VOL. 65, 1999 COMMUNITY SIZE AND RATES OF ARCTIC SULFATE REDUCERS 4231

shown). These differences indicate that psychrophilic SRB are
adapted to low temperatures not only because their minimum
growth temperatures are at or below in situ temperatures but
also because their metabolic rates are comparable to those of
mesophiles at temperatures 6 to 10°C higher. Many studies
have demonstrated that organisms active at low temperature
differ physiologically from their counterparts in warmer envi-
ronments (reference 22 and references therein). Cell mem-
branes of psychrophiles tend to contain more unsaturated fatty
acids (3, 5) and short-chain fatty acids (3) than membranes of
mesophiles. Changes in the membrane composition might lead
to a more efficient solute uptake at low temperatures (23).
Furthermore, psychrophiles synthesize enzymes with high cat-
alytic activities at low temperatures (8) and produce more
enzymes when the temperature decreases (7). Different en-
zymes or enzyme levels could be one explanation for the com-
parable SRRs for psychrophiles and mesophiles at different
temperatures.
The calculated activation energy (E
a
) of mesophilic SRB was
90.6 kJ/mol, which is within the range (23 to 132 kJ/mol)
determined previously for sulfate reduction in temperate sed-
iments (1, 6, 29) and close to the values (74 and 85 kJ/mol)
calculated from specific SRR between 0 and 30°C for a Desul-
fovibrio desulfuricans strain (15). Thus, we suppose that the
specific SRRs measured in pure cultures are representative for
mesophilic sulfate reducers of temperate sediments. However,
the possibility that measured rates for mesophiles were biased
by the inability of most strains to grow at the low experimental
temperatures cannot be ruled out. This problem could not be
avoided in our use of culture collection strains because meso-
philic marine sulfate reducers that are able to grow at temper-
ature as low as 0°C are almost unknown.
TABLE 1. Growth characteristics and specific SRRs of psychrophilic SRB measured at the in situ temperatures of their habitats
Strain Substrate
a
Incubation
temp (°C)
Specific SRR
(fmol cell
⫺1
day
⫺1
)
Growth at each temp (°C)
⫺1.8 4 15 20 26
Hornsund
LSv20 Lactate 2.6 14.0 ⫾ 0.6 ⫹⫹ ⫹ ⫹⫺
LSv21 Lactate 2.6 2.7 ⫾ 0.7 ⫹⫹ ⫹ ⫹⫺
LSv22 Lactate 2.6 13.0 ⫾ 2.0 ⫹⫹ ⫹ ⫹⫹
LSv23 Lactate 2.6 2.3 ⫾ 0.6 ⫹⫹ ⫹ ⫹⫺
LSv24 Lactate 2.6 11.0 ⫾ 0.8 ⫹⫹ ⫹ ⫹⫺
LSv25 Lactate 2.6 2.8 ⫾ 1.1 ⫹⫹ ⫹ ⫹⫺
LSv26 Lactate 2.6 6.9 ⫾ 0.5 ⫹⫹ ⫹ ⫹⫹
LSv27 Lactate 2.6 2.6 ⫾ 0.3 ⫹⫹N.D.
b
⫺⫺
LSv28 Lactate 2.6 2.6 ⫾ 0.2 ⫹⫹ ⫹ ⫺⫺
PlSv28 Propanol 2.6 2.5 ⫾ 1.4 ⫹⫹ ⫹ ⫺⫺
PSv29 Propionate 2.6 41.9 ⫾ 23.4 ⫹⫹ ⫺ ⫺⫺
ASv25 Acetate 2.6 25.3 ⫾ 0.3 ⫹⫹ ⫹ ⫹⫺
ASv26 Acetate 2.6 3.8 ⫾ 1.0 ⫹⫹ ⫺ ⫺⫺
ASv28 Acetate 2.6 11.3 ⫾ 0.9 ⫹⫹ ⫹ ⫹⫹
Storfjord
LSv514 Lactate ⫺1.7 3.6 ⫾ 0.4 ⫹⫹ ⫹ ⫹⫺
LSv52 Lactate ⫺1.7 7.6 ⫾ 3.7 ⫹⫹ ⫹ ⫹⫺
LSv53 Lactate ⫺1.7 0.9 ⫾ 0.4 ⫹⫹ ⫹ ⫹⫺
LSv54 Lactate ⫺1.7 1.9 ⫾ 0.2 ⫹⫹ ⫹ ⫺⫺
LSv55 Lactate ⫺1.7 6.2 ⫾ 0.8 ⫹⫹ ⫹ ⫺⫺
a
Carbon substrate used for isolation and for measurements of specific SRRs.
b
N.D., not determined.
c
Values are means ⫾ standard deviations for three cultures. The mean specific SRRs were 10.2 and 4.0 fmol cell
⫺1
day
⫺1
for the Hornsund strains and Storfjord
strains, respectively.
TABLE 2. Specific SRRs of mesophilic SRB at different temperatures
Strain
DSMZ
a
strain no.
Substrate
b
Specific SRR (fmol cell
⫺1
day
⫺1
)
c
at:
4°C 8°C 13°C
Desulfobacter postgatei 2043 Acetate 11.0 ⫾ 1.6 19.4 ⫾ 1.4 37.9 ⫾ 5.9
D. hydrogenophilus 3380 Hydrogen 8.0 ⫾ 0.3 7.8 ⫾ 2.8 20.0 ⫾ 3.3
Desulfobulbus sp. 3pr10 2058 Propionate 4.2 ⫾ 0.1 6.2 ⫾ 0.36 12.2 ⫾ 0.6
Desulfovibrio salexigens 2636 Lactate 0.7 ⫾ 0.06 1.4 ⫾ 0.07 3.9 ⫾ 0.4
Desulfovibrio vulgaris 1744 Lactate 0.4 ⫾ 0.05 0.8 ⫾ 0.06 2.1 ⫾ 0.1
Desulfobacterium autotrophicum 3382 Lactate 1.6 ⫾ 0.07 2.9 ⫾ 0.2 4.4 ⫾ 0.4
Desulfofustis glycolicus 9705 Glycolate 0.3 ⫾ 0.01 0.5 ⫾ 0.06 1.1 ⫾ 0.1
Desulfococcus niacini 2650 Nicotinate 1.2 ⫾ 0.05 2.0 ⫾ 0.24 4.0 ⫾ 0.7
Desulfosarcina variabilis 2060 Benzoate 0.7 ⫾ 0.4 9.0 ⫾ 2.3 20.0 ⫾ 0.6
a
All strains were obtained from the Deutsche Sammlung fu¨r Mikroorganismen und Zellkulturen (DSMZ), Braunschweig, Germany.
b
Carbon substrates used for isolation and for measurements of specific SRRs.
c
Values are means ⫾ standard deviations for three cultures. The mean specific SRRs were 3.1, 5.6, and 11.7 fmol cell
⫺1
day
⫺1
at 4, 8, and 13°C, respectively.
Measurements of specific SRR were made in 15-ml Hungate tubes except for D. hydrogenophilus, which was incubated in flat 50-ml culture flasks to enhance hydrogen
diffusion into the aqueous phase.
4232 KNOBLAUCH ET AL. APPL.ENVIRON.MICROBIOL.

We thank the cruise leader, Donald E. Canfield, and the crew of the
RV Jan Mayen for a successful Svalbard cruise. We are grateful to
Kerstin Sahm and Friedrich Widdel for help during the isolation of the
studied strains and for critical discussions and to Bo Thamdrup for
help with the computer software.
This work was supported by the Max Planck Society, Germany.
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FIG. 2. Mean values of specific SRRs of 10 mesophilic sulfate reducers
(closed circles) determined at 4, 8, and 13°C, 14 psychrophiles from Hornsund
sediments (open square), and 5 psychrophiles from Storfjord sediments (open
triangle). Dashed line represents the Arrhenius fit of specific SRRs for meso-
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VOL. 65, 1999 COMMUNITY SIZE AND RATES OF ARCTIC SULFATE REDUCERS 4233