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


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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.
Content may be subject to copyright.
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
Departments of Biogeochemistry
and Microbiology,
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 1.7°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
Two permanently cold sediments, located off the coast of
Svalbard, Hornsund (76°582N, 15°345E; in situ tempera-
ture, 2.6°C) and Storfjord (77°330N, 19°050E; 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
cells cm
for Hornsund sediments (Fig. 1b), are in the range
of those reported previously for temperate marine sediments
(2 10
to 2 10
cells cm
(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
must be comparable too, irrespective of the temperature dif-
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
(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 exp(E
[R T]
), where A is a constant, E
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;
, 10°C;
, 4°C) or acetate (
, 20°C;
, 10°C;
, 4°C). Horizontal bars represent 95% confidence intervals, and vertical bars indicate the depths of sediments used for MPN enrichments.
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
The calculated activation energy (E
) 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
temp (°C)
Specific SRR
(fmol cell
Growth at each temp (°C)
1.8 4 15 20 26
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.
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 ⫹⫹
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 ⫹⫹
Carbon substrate used for isolation and for measurements of specific SRRs.
N.D., not determined.
Values are means standard deviations for three cultures. The mean specific SRRs were 10.2 and 4.0 fmol cell
for the Hornsund strains and Storfjord
strains, respectively.
TABLE 2. Specific SRRs of mesophilic SRB at different temperatures
strain no.
Specific SRR (fmol cell
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
All strains were obtained from the Deutsche Sammlung fu¨r Mikroorganismen und Zellkulturen (DSMZ), Braunschweig, Germany.
Carbon substrates used for isolation and for measurements of specific SRRs.
Values are means standard deviations for three cultures. The mean specific SRRs were 3.1, 5.6, and 11.7 fmol cell
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.
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.
1. Aller, R. C., and J. Y. Yingst. 1980. Relationships between microbial distri-
butions and the anaerobic decomposition of organic matter in surface sed-
iments of Long Island Sound, USA. Mar. Biol. 56:29–42.
2. American Public Health Association. 1969. Standard methods for the exam-
ination of water and wastewater, including bottom sediment and sludge.
American Public Health Association, Washington, D.C.
3. Bhakoo, M., and R. A. Herbert. 1979. The effects of temperature on the fatty
acid and phospholipid composition of four obligately psychrophilic Vibrio
spp. Arch. Microbiol. 121:121–127.
4. Canfield, D. E., B. B. Jørgensen, H. Fossing, R. Glud, J. Gundersen, N. B.
Ramsing, B. Thamdrup, J. W. Hansen, L. P. Nielsen, and P. O. J. Hall. 1993.
Pathways of organic carbon oxidation in three continental margin sediments.
Mar. Geol. 113:27–40.
5. Chan, M., R. H. Himes, and J. M. Akagi. 1971. Fatty acid composition of
thermophilic, mesophilic, and psychrophilic clostridia. J. Bacteriol. 106:876–
6. Crill, P. M., and C. S. Martens. 1987. Biogeochemical cycling in an organic-
rich coastal marine basin. 6. Temporal and spatial variations in sulfate
reduction rates. Geochim. Cosmochim. Acta 51:1175–1186.
7. Feller, G., E. Narinx, J. L. Arpigny, Z. Zekhnini, J. Swings, and C. Gerday.
1994. Temperature dependence of growth, enzyme secretion and activity of
psychrophilic Antarctic bacteria. Appl. Microbiol. Biotechnol. 41:477–479.
8. Feller, G., F. Payan, F. Theys, M. Qian, R. Haser, and C. Gerday. 1994.
Stability and structural analysis of -amylase from the Antarctic psychrophile
Alteromonas haloplanctis A23. Eur. J. Biochem. 222:441–447.
9. Isaksen, M. F., and B. B. Jørgensen. 1996. Adaptation of psychrophilic and
psychrotrophic sulfate-reducing bacteria to permanently cold marine envi-
ronments. Appl. Environ. Microbiol. 62:408–414.
10. Isaksen, M. F., and A. Teske. 1996. Desulforhopalus vacuolatus gen. nov., sp.
nov., a new moderately psychrophilic sulfate-reducing bacterium with gas
vacuoles isolated from a temperate estuary. Arch. Microbiol. 166:160–168.
11. Jørgensen, B. B. 1978. A comparison of methods for the quantification of
bacterial sulfate reduction in coastal marine sediments I. Measurement with
radiotracer techniques. Geomicrobiol. J. 1:11–27.
12. Jørgensen, B. B. 1982. Mineralization of organic matter in the sea bed—the
role of sulphate reduction. Nature 296:643–645.
13. Jørgensen, B. B., and F. Bak. 1991. Pathways and microbiology of thiosulfate
transformations and sulfate reduction in a marine sediment (Kattegat, Den-
mark). Appl. Environ. Microbiol. 57:847–856.
14. Jørgensen, B. B., M. Bang, and T. H. Blackburn. 1990. Anaerobic mineral-
ization in marine sediments from the Baltic Sea-North Sea transition. Mar.
Ecol. Prog. Ser. 59:39–54.
15. Kaplan, I. R., and S. C. Rittenberg. 1964. Microbiological fractionation of
sulphur isotopes. J. Gen. Microbiol. 34:195–212.
16. Knoblauch, C., and B. B. Jørgensen. Effect of temperature on sulfate reduc-
tion, growth rate, and growth yield in five psychrophilic sulfate-reducing
bacteria from Arctic sediments. In Environmental Microbiology, vol. 1, in
press. Blackwell Science, Ltd., Oxford, United Kingdom.
17. Knoblauch, C., K. Sahm, and B. B. Jørgensen. Psychrophilic sulfate-reduc-
ing bacteria isolated from permanently cold Arctic marine sediments: de-
scription of Desulfofrigus oceanense gen. nov., sp. nov., Desulfofrigus fragile sp.
nov., Desulfofaba gelida gen. nov., sp. nov., Desulfotalea psychrophila gen.
nov., sp. nov., and Desulfotalea arctica, sp. nov. Int. J. Syst. Bacteriol., in
18. Kostka, J. E., B. Thamdrup, R. N. Glud, and D. E. Canfield. 1999. Rates and
pathways of carbon oxidation in permanently cold Arctic sediments. Mar.
Ecol. Prog. Ser. 180:7–21.
19. Levitus, S., and T. Boyer. 1994. World ocean atlas, vol. 4: Temperature. U.S.
Department of Commerce, Washington, D.C.
20. Lillebæk, R. 1995. Application of antisera raised against sulfate-reducing
bacteria for indirect immunofluorescent detection of immunoreactive bac-
teria in sediment from the German Baltic Sea. Appl. Environ. Microbiol.
21. Nedwell, D. B., T. R. Walker, J. C. Ellis-Evans, and A. Clarke. 1993. Mea-
surements of seasonal rates and annual budgets of organic carbon fluxes in
an Antarctic coastal environment at Signy Island, South Orkney Islands,
suggest a broad balance between production and decomposition. Appl. En-
viron. Microbiol. 59:3989–3995.
22. Russell, N. J., and T. Hamamoto. 1998. Psychrophiles, p. 25–45. In K.
Horikoshi and W. D. Grant (ed.), Extremophiles: microbial life in extreme
environments. John Wiley & Sons, New York, N.Y.
23. Russell, N. J. 1990. Cold adaptation of microorganisms. Philos. Trans. R.
Soc. Lond. B Biol. Sci. 326:595–611.
24. Sagemann, J., B. B. Jørgensen, and O. Greef. 1998. Temperature depen-
dence and rates of sulfate reduction in cold sediments of Svalbard, Arctic
Ocean. Geomicrobiol. J. 15:85–100.
25. Sahm, K., C. Knoblauch, and R. I. Amann. 1999. Phylogenetic affiliation and
quantification of psychrophilic sulfate-reducing isolates in marine Arctic
sediments. Appl. Environ. Microbiol. 65:3976–3981.
26. Sahm, K., B. J. MacGregor, B. B. Jørgensen, and D. A. Stahl. 1999. Sulphate
reduction and vertical distribution of sulphate-reducing bacteria quantified
by rRNA slot-blot hybridization in a coastal marine sediment. Environ.
Microbiol. 1:65–74.
27. Teske, A., C. Wawer, G. Muyzer, and N. B. Ramsing. 1996. Distribution of
sulfate-reducing bacteria in a stratified fjord (Mariager Fjord, Denmark) as
evaluated by most-probable-number counts and denaturing gradient gel
electrophoresis of PCR-amplified ribosomal DNA fragments. Appl. Environ.
Microbiol. 62:1405–1415.
28. Thamdrup, B., H. Fossing, and B. B. Jørgensen. 1994. Manganese, iron, and
sulfur cycling in a coastal marine sediment, Aarhus Bay, Denmark. Geochim.
Cosmochim. Acta 58:5115–5129.
29. Westrich, J. T., and R. A. Berner. 1988. The effect of temperature on rates
of sulfate reduction in marine sediments. Geomicrobiol. J. 6:99–117.
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-
philes. Bars represent standard deviations of the means for all strains.
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... Sulfate reduction was activated in all −5°C conditions compared to the control, demonstrating a cold-adapted sulfate metabolic response in Cp34H. Sulfate reduction has been previously noted to be more active in psychrophilic marine bacteria compared to warmer-adapted marine bacteria (Knoblauch et al., 1999a;Knoblauch et al., 1999b) and general carbon turnover rates in Arctic marine sediments are comparable to temperate climates due to their activity (Sageman et al., 1998). This, however, is the first analysis to reveal that sulfate reduction enzymes in a psychrophilic bacterium increased in response to lower subzero temperatures (i.e., −1°C to −5°C) regardless of nutrient input (CysC, CysJ, CysI, CysH, CysN, CysD, Fig. 5A-D; Dataset S9). ...
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Colwellia psychrerythraea is a marine psychrophilic bacterium known for its remarkable ability to maintain activity during long‐term exposure to extreme subzero temperatures and correspondingly high salinities in sea ice. These microorganisms must have adaptations to both high salinity and low temperature to survive, be metabolically active, or grow in the ice. Here, we report on an experimental design that allowed us to monitor culturability, cell abundance, activity, and proteomic signatures of Colwellia psychrerythraea strain 34H (Cp34H) in subzero brines and supercooled sea water through long‐term incubations under eight conditions with varying subzero temperatures, salinities, and nutrient additions. Shotgun proteomics found novel metabolic strategies used to maintain culturability in response to each independent experimental variable, particularly in pathways regulating carbon, nitrogen, and fatty acid metabolism. Statistical analysis of abundances of proteins uniquely identified in isolated conditions provide metabolism‐specific protein biosignatures indicative of growth or survival in either increased salinity, decreased temperature, or nutrient limitation. Additionally, to aid in the search for extant life on other icy worlds, analysis of detected short peptides in ‐10°C incubations after four months identified over 500 potential biosignatures that could indicate the presence of terrestrial‐like cold‐active or halophilic metabolisms on other icy worlds. This article is protected by copyright. All rights reserved.
Thesis (Ph. D. in Molecular Biology, Microbiology, and Biochemistry, MBMB program)--Southern Illinois University Carbondale, 2006.
This chapter reviews the environmental and ecological activities of the SRB in greatest abundance in the terrestrial microbiome as well as the unique SRP reported in only a few environmental sites. Dissimilatory sulfate reduction is the hallmark characteristic of SRB, and wherever sulfate is found, SRB are found. SRB inhabit temperate zone but also are found in the extreme environments of the earth, which include pH, temperature and pressure extremes, and elevated salt concentrations. Sulfate-respiring microorganisms are found throughout the biosphere, and they display considerable adaptation to that environment. The physiological capabilities and adaptability of SRB indicate the influence of SRB on ecological transformations in the biosphere.KeywordsExtremophiles Thermophiles Halophiles Psychrophiles Acidophiles Piezophiles
The sulfate-reducing bacteria (SRB) are chemolithotrophic organisms with an array of redox active enzymes and they have a major impact on the carbon, sulfur, and nitrogen global cycles. This chapter reviews the decomposition of complex and low-molecular-weight hydrocarbons. As a product of respiration, hydrogen sulfide impacts the oil industry, agriculture, mining industry, and geochemical environment. This chapter summarizes reduction of metals, metalloids, and radionuclides by SRB with attention given to the use of SRB to detoxify the environment. Additionally, the formation of metallic nanoparticles by SRB is discussed. Several industrial applications involving SRB are discussed including energy technology and decolorization of textile dyes.KeywordsMercury methylationNanoparticlesChlorate decompositionAcid mine watersCarbon cyclingDecomposition of petroleum hydrocarbonsBioremediation
Climate-induced changes in the composition of organic matter sources in Chukchi Sea sediments could have major implications on carbon cycling, carbon sequestration, and food sources for lower benthic trophic levels. The aim of this study was two-fold: (1) to identify the proportional contributions of organic matter from various primary producers (phytoplankton, terrestrial, and bacterial) to depth-stratified sediments (0–5 cm) across the Arctic Chukchi Sea shelf using essential amino acid (EAA) specific stable carbon isotope biomarkers; and (2) to experimentally evaluate sediment bacterial production under different temperature scenarios. Proportional contributions of EAA sources to surface sediments had little relationship with environmental variables across the Chukchi Shelf and only showed noticeably higher terrestrial proportions in surface sediments in a high-deposition region in the southern study area. Across all sediment depth strata, the majority of EAA in sediments (∼76%) originated from terrestrial sources and may be indicative of accumulation over time due to slow degradation processes of this source within sediments. The different EAA sources showed no significant differences in proportional contributions with sediment depth except for phytoplankton-derived EAA, which decreased with increasing sediment depth. These patterns indicate a well-mixed upper sediment horizon, possibly from bioturbation activities by the abundant benthos. One EAA source assumed to respond quickly to changing environmental conditions are bacteria. To evaluate if and how bacterial production would respond to elevated temperatures, sediment bacterial production was measured experimentally using phospholipid fatty acid (PLFA) analysis. Bacterial production was initially (first 24 h) higher at 5 °C than at 0 °C; however, a drawdown of substrate or potential increase in predation activity and viral lysis resulted in bacterial production to subsequently be similar at both temperature settings. Overall results of this study suggest that terrestrial and bacterial carbon sources may become more prominent in a future, warmer Arctic. Identifying current patterns and potential shifts in organic matter sources with changes in temperature can aid in the understanding of the consequences of climate change in terms of organic matter presence and flow through benthic consumers that use these shelf sediments as feeding grounds.
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Serpentinization of peridotites in Earth’s mantle is associated with the generation of hydrogen and low molecular weight organics that could support subsurface life. Studies of microbial metabolisms in peridotite-hosted environments have focused primarily on methanogenesis, yet DNA sequences, isotopic composition of sulfides and thermodynamic calculations suggest there is potential for microbial sulfate reduction too. Here, we use a sulfate radiotracer-based method to quantify microbial sulfate reduction rates in serpentinization fluids recovered from boreholes in the Samail Ophiolite, Oman and the California Coast Range Ophiolite, USA. We find that low levels of sulfate reduction occur at pH up to 12.3. These low levels could not be stimulated by addition of hydrogen, methane or small organic acids, which indicates that this metabolism is limited by factors other than substrate availability. Cellular activity drops at pH > 10.5 which suggests that high fluid pH exerts a strong control on sulfate-reducing organisms in peridotites.
Microorganisms in the seabed of most of the global oceans live at temperatures close to zero degrees, and in the polar regions even below. Respiration rates of endogenous sulfate‐reducing microorganisms in the polar seabed, however, are highest in the range of 18–30°C and much reduced at colder temperature. In the past, this was seen as indicative of poor adaptation to their cold habitat. We challenge this interpretation, and tested which temperature range allowed sulfate reducers to grow, by adding moderate amounts of volatile fatty acids to high‐arctic sediment. Initially, sulfate reduction was highest at 27°C in both Svalbard and NE Greenland. But sulfate reduction was not sustainable at this temperature and decreased rapidly over time. Below 26°C, however, sulfate reduction rates increased exponentially over time, indicating growth of sulfate‐reducing microorganisms. We used the increase in the sulfate reduction rates over 4 d to calculate potential growth rates of the endogenous sulfate reducers as function of temperature. From growth rates and respiration rates, we could further calculate the growth yield, also as function of temperature. Highest growth rates were observed at 18°C and growth yields peaked at even lower temperatures between 0°C and 10°C. The maximum growth yield at low temperature revealed a strong psychrophilic adaptation of the sulfate reducers in these Arctic sediments. The fact that growth yield was maximized at in situ temperature but maximum potential growth rate was not, is an indication that yield is the more important parameter for microbial competition in marine sediments.
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We report her-e a comprehensive study of the rates and pathways of carbon mineralization in Arctic sediments. Four sites were studied at 115 to 329 m water depth in fjords on Svalbard and in coastal Norway. The Svalbard coastal region is characterized by permanently cold bottom water temperatures of -1.7 to 2.6 degrees C. Carbon oxidation (avg = 20 to 400 nmol cm(-3) d(-1)) and sulfate reduction rates (avg = 10 to 350 nmol cm(-3) d(-1)) were measured at high resolution to 10 cm depth in sediment incubations. The distribution of oxidants available for microbial respiration was determined through porewater and solid phase geochemistry. By comparing the distribution of potential oxidants to the depth-integrated mineralization rates, the importance of various respiratory pathways to the oxidation of organic C could be quantified. Integrated C oxidation rates measured in sediment incubations (11 to 24 mmol m(-2) d(-1)) were comparable to within a factor of 2 to dissolved inorganic carbon (DIC) fluxes measured in situ using a benthic lander. Sulfate reduction was the dominant microbial respiration pathway (58 to 92% of total C oxidation) followed by Fe(III) reduction (10 to 26%), oxygen (5 to 14%), and nitrate respiration (2 to 3%). At sediment depths where sulfate reduction was dominant, C oxidation equivalents, calculated from independently measured sulfate reduction rates, matched DIC production rates in incubations. Sediment geochemistry revealed that the same vertical sequence of oxidants is reduced/respired in these Arctic sediments as in temperate continental shelf sediments of equivalent water depths. Microbial communities in permanently cold Arctic sediments exhibited mineralization rates and pathways comparable to temperate nearshore environments. This study completely partitioned C oxidation pathways, showing a predominance of sulfate respiration and a substantial contribution of Fe(III) reduction to organic matter mineralization in Arctic sediments for the first time. Microbial communities in cold sediments exposed to relatively high C deposition appear to respond to the input or availability of organic matter rather than to temperature.
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Psychrophilic and psychrotrophic microorganisms are important in global ecology as a large proportion of our planet is cold (below 5 ⚬C); they are responsible for the spoilage of chilled food and they also have potential uses in low-temperature biotechnological processes. Psychrophiles and psychrotrophs are both capable of growing at or close to zero, but the optimum and upper temperature limits for growth are lower for psychrophiles compared with psychrotrophs. Psychrophiles are more often isolated from permanently cold habitats, whereas psychrotrophs tend to dominate those environments that undergo thermal fluctuations. The molecular basis of psychrophily is reviewed in terms of biochemical mechanisms. The lower growth temperature limit is fixed by the freezing properties of dilute aqueous solutions inside and outside the cell. In contrast, the ability of psychrophiles and psychrotrophs to grow at low, but not moderate, temperatures depends on adaptive changes in cellular proteins and lipids. Changes in proteins are genotypic, and are related to the properties of enzymes and translation systems, whereas changes in lipids are genotypic or phenotypic and are important in regulating membrane fluidity and permeability. The ability to adapt their solute uptake systems through membrane lipid modulation may distinguish psychrophiles from psychrotrophs. The upper growth temperature limit can result from the inactivation of a single enzyme type or system, including protein synthesis or energy generation.
The potential for sulfate reduction at low temperatures was examined in two different cold marine sediments, Mariager Fjord (Denmark), which is permanently cold (3 to 6(deg)C) but surrounded by seasonally warmer environments, and the Weddell Sea (Antarctica), which is permanently below 0(deg)C. The rates of sulfate reduction were measured by the (sup35)SO(inf4)(sup2-) tracer technique at different experimental temperatures in sediment slurries. In sediment slurries from Mariager Fjord, sulfate reduction showed a mesophilic temperature response which was comparable to that of other temperate environments. In sediment slurries from Antarctica, the metabolic activity of psychrotrophic bacteria was observed with a respiration optimum at 18 to 19(deg)C during short-term incubations. However, over a 1-week incubation, the highest respiration rate was observed at 12.5(deg)C. Growth of the bacterial population at the optimal growth temperature could be an explanation for the low temperature optimum of the measured sulfate reduction. The potential for sulfate reduction was highest at temperatures well above the in situ temperature in all experiments. The results from sediment incubations were compared with those obtained from pure cultures of sulfate-reducing bacteria by using the psychrotrophic strain ltk10 and the mesophilic strain ak30. The psychrotrophic strain reduced sulfate optimally at 28(deg)C in short-term incubations, even though it could not grow at temperatures above 24(deg)C. Furthermore, this strain showed its highest growth yield between 0 and 12(deg)C. In contrast, the mesophilic strain ak30 respired and grew optimally and showed its highest growth yield at 30 to 35(deg)C.
This atlas contains maps of in situ temperature at selected levels of the world ocean on a one-degree grid. Maps for all-data annual and seasonal compositing periods are presented. The fields used to generate these maps were computed by objective analysis of historical data. Data distribution maps are presented for various compositing periods including monthly distributions. Basin zonal averages and basin volume averages are computed from these objectively analyzed fields and presented in the form of figures and tables.
Rates of sulfate reduction in sediments of Long Island Sound have been determined, as a function of temperature, via the S radiotracer method. Temperature dependence was measured either by following changes in rates in intact cores with seasonal changes in temperature, or by conducting laboratory experiments on homogenized sediments under controlled temperatures. At constant temperature, a large range of sulfate reduction rates were observed for the study sites. In both the intact cores and the laboratory experiments, sediments with lower rates of sulfate reduction exhibited a more pronounced temperature dependence. Apparent activation energies determined using the Arrhenius equation show a systematic trend with sulfate reduction rate when temperature was normalized. As the rate of sulfate reduction decreased, the apparent activation energy increased from 36 to 132 kJ/mole. Although this observation can be interpreted in a number of ways, it is suggested that susceptibility of organic matter to metabolic attack exerts an important control on the temperature dependence of sulfate reduction, as well as on the rate itself. Our findings indicate that the use of a constant temperature correction for estimating annual rates of sulfate reduction will be inaccurate.
The free fatty acid and phospholipid composition of 4 psychrophilic marineVibrio spp. have been determined in chemostat culture with glucose as the limiting substrate over a temperature range 0–20°C. All the isolates show maximum glucose and lactose uptake at 0°C and this correlates with maximum cell yield. None of the isolates contain fatty acids with a chain length exceeding 17 carbon atoms.Vibrio AF-1 andVibrio AM-1 respond to decreased growth temperatures by synthesizing increased proportions of unsaturated fatty acids (C15:1, C16:1 and C17:1) whereas inVibrio BM-2 the fatty acids undergo chain length shortening. The fourth isolate (Vibrio BM-4) contains high levels (60%) of hexadecenoic acid at all growth temperatures and the fatty acid composition changes little with decreasing temperature. The principal phospholipid components of the four psychrophilic vibrios were phosphatidylserine, phosphatidylglycerol, phosphatidylethanolamine and diphosphatidylglycerol. Lyso-phosphatidylethanolamine and 2 unknown phospholipids were additionally found inVibrio AF-1. The most profound effect of temperature on the phospholipid composition of these organisms was the marked increase in the total quantities synthesized at 0°C. At 15°C phosphatidylglycerol accumulated in the isolates as diphosphatidylglycerol levels decreased. Additionally inVibrio BM-2 andVibro BM-4 phosphatidylserine accumulates as phosphatidylethanolamine biosynthesis was similarly impaired. The observed changes in fatty acid and phospholipid composition in these organisms at 0°C may explain how solute transport is maintained at low temperature.