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J Bacteriol, May 1998, p. 2770-2774, Vol. 180, No. 10
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Acquired Thermotolerance and Temperature-Induced
Protein Accumulation in the Extremely Thermophilic Bacterium
Rhodothermus obamensis
Ken
Takai,1,2,*
Takuro
Nunoura,1
Yoshihiko
Sako,1 and
Aritsune
Uchida1
Laboratory of Marine Microbiology, Division
of Applied Bioscience, Graduate School of Agriculture, Kyoto
University, Kyoto 606-01,1 and
Deep-Sea
Microorganisms Research Group, Japan Marine Science and Technology
Center, Yokosuka 237,2 Japan
Received 17 November 1997/Accepted 16 March 1998
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ABSTRACT |
Temperature-induced changes in thermotolerance and protein
composition were examined in heat-shocked cells and
high-temperature-grown cells of the extremely thermophilic bacterium
Rhodothermus obamensis. The survival at temperatures
superoptimal for growth (90 and 95°C) was enhanced in both
heat-shocked cells and high-temperature-grown cells relative to that of
cells grown at optimal temperatures. In a comparison of protein
composition using two-dimensional gel electrophoresis, putative heat
shock proteins (HSPs) and high-temperature growth-specific proteins
(HGPs) were detected. N-terminal amino acid sequence analysis revealed
that the putative HSPs were quite similar to the ATP-binding
subunits of ABC transporters and the HGPs were proteins corresponding
to domains II and III of elongation factor Tu. These results suggested
that this extreme thermophile has developed temperature-induced
responses that include increased survival under hyperthermal
conditions, changes in protein composition, and also the production of
novel HSPs.
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TEXT |
The heat shock response is a stress
response mechanism found in various organisms from Escherichia
coli to mammals and involves the increased synthesis of proteins
which protect an organism from thermal stress (22, 25). The
nature of the heat shock response of extremely thermophilic
microorganisms, which grow at temperatures of above 80°C, is
intriguing, considering the fact that they thrive at temperatures far
above the limits for most cells (9, 36). In some organisms,
thermal stress induces not only synthesis of specific proteins but also
elevated levels of certain intracellular compatible solutes (8,
15, 23, 33, 40).
Most work to date on heat shock and thermal acclimation in thermophilic
microorganisms has focused on members of the domain Archaea.
Holden and Baross found enhanced thermotolerance and increased levels
of a 98-kDa protein in the hyperthermophilic archaeon ES4 when its
growth temperature was shifted from 95 to 102°C (18).
Another hyperthermophile, Pyrodictium occultum, produced
increased levels of an ATPase complex (i.e., thermosome) when the
culture temperature was shifted from 102 to 108°C (28, 29), and a similar ATPase complex has been identified in
Thermoplasma acidophilum (39). In the members of
the order Sulfolobales, prominent heat shock proteins with
subunit molecular masses of approximately 60 kDa have been reported
(36). These major heat shock proteins are thermophilic
factor 55 and its relatives and are similar to a eukaryotic protein
family known as t-complex polypeptide 1 (13, 21, 27, 34,
35). It has also been suggested that these proteins are involved
in the heat shock response and thermal acclimation in the
thermoacidophilic archaea (11).
Given that the heat shock response and thermal acclimation are
ubiquitous mechanisms in the extremely thermophilic microorganisms, the
mechanism in extremely thermophilic bacteria represents an interesting
model that can be compared with the archaeal mechanism. Rhodothermus obamensis is an extremely thermophilic
bacterium, growing at temperatures between 55 and
85°C, that was recently isolated by Sako et al. from a shallow marine
hydrothermal vent in Japan (32). In this study, we sought to
determine the thermal acclimation of heat-shocked and
high-temperature-grown R. obamensis cells.
Temperature-induced changes in protein composition were examined,
and the possible function of the novel heat shock protein-like proteins
is discussed.
Morphological changes and acquired thermotolerance.
The
bacterial strain used in this study was R. obamensis OKD7
(JCM 9785), which was isolated by Sako et al. from a shallow marine
hydrothermal vent at Tachibana Bay, Nagasaki Prefecture, Japan
(32). For the cultivation of R. obamensis, Jx
medium was used (32). R. obamensis was grown at
76°C and harvested in the midexponential growth phase
(optimal-temperature-grown cells), grown at 76°C until the
midexponential growth phase, and then incubated at 88°C for
1 h (heat-shocked cells), or grown at 84°C and harvested
in the midexponential growth phase (high-temperature-grown cells). The
heat shock at 88°C for 1 h had little effect on cell viability,
and the temperature of 84°C was approximately the maximal temperature
that permits growth. Cells in the midexponential growth phase at 84°C
are smaller than those grown at 76°C (Fig.
1) and have diminished cell pigments
(data not shown). It has been reported that mesophilic bacteria such as
Vibrio spp. reduce their cell size or volume under
starvation stress and oligotrophic conditions, and it has been
suggested that the reduced size or volume is involved in the adaptation
to the unusual growth conditions (19, 26). It seems likely,
therefore, that the morphological changes in high-temperature-grown
cells are also involved in thermal acclimation under hyperthermal
conditions.
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FIG. 1.
Differential interference micrographs of R. obamensis cells. (A) Cells growing exponentially at the optimum
temperature of 76°C. (B) Cells growing exponentially at approximately
the maximal temperature of 84°C. Bars, 5 µm.
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To determine the ability of R. obamensis to withstand
hyperthermal conditions, optimum-temperature-grown,
heat-shocked, or high-temperature-grown cells were rapidly
exposed to lethal temperatures of 90 and 95°C (Fig.
2). The numbers of intact cells and
viable cells were estimated by an epifluorescence microscopic method using 4',6-diamidino-2-phenylindole (30) and by the
five-tube most-probable-number technique (2), respectively.
Although the total cell counts were constant during the exposure to
lethal temperatures, viable cell counts decreased with increasing
exposure time. The thermal death curve experiments with
optimum-temperature-grown, heat-shocked, and high-temperature-grown
cells revealed different levels of thermotolerance. The
optimum-temperature-grown cells demonstrated an exponential decrease in
viability at both 90 and 95°C, and the heat-shocked cell displayed a
significantly lower death rate and transient thermotolerance (Fig. 2).
The exponential rate of decline was increased after 30 min at 90°C or
after 5 min at 95°C. The cells grown at 84°C were most
thermotolerant and were successfully acclimated to hyperthermal
conditions. Acquired thermotolerance has been reported in the
hyperthermophilic archaeon ES4 and in the extremely thermoacidophilic
archaea Sulfolobus shibatae and Metallosphaera
sedula (18, 27, 34). In these archaea, thermal
acclimation was promoted by prior incubation at temperatures close to
the maximum growth temperature for the organisms and was accompanied by
the increased synthesis of some proteins. It seems likely that the
increased thermotolerance in high-temperature-grown or heat-shocked
cells is ubiquitous in the thermophilic microorganisms and represents a
possible mechanism for survival under hyperthermal conditions.
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FIG. 2.
Thermal-death curves for optimum-temperature-grown cells
( ), heat-shocked cells ( ), and high-temperature-grown cells ( )
of R. obamensis exposed to 90°C (A) or 95°C (B). The
numbers of viable cells were estimated by the five-tube
most-probable-number technique. Error bars represent the 95%
confidence interval for each point.
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Protein composition variations with temperature changes.
The protein composition was analyzed by two-dimensional (2-D)
electrophoresis in optimal-temperature-grown, heat-shocked, and
high-temperature-grown cells. Each culture was collected by centrifugation and washed twice with 50 mM Tris-HCl (pH 8.0). The cells
were resuspended in lysis buffer containing 9 M urea, 2% (vol/vol)
Triton X-100, 2% (vol/vol) 2-mercaptoethanol, and 0.8% ampholine (pH
3.5 to 9.5; Pharmacia), and ruptured by ultrasonication. The cell
lysate was centrifuged at 15,000 × g for 10 min, and the protein was precipitated from the supernatant by 5% (wt/vol) trichloroacetic acid. The protein pellet was resuspended with sample
buffer containing 8 M urea, 0.5% (vol/vol) Triton X-100, 2% (vol/vol)
2-mercaptoethanol, 0.8% ampholine (pH 3.5 to 9.5; Pharmacia), and
0.01% bromophenol blue, and equal amounts of proteins (50 µg) were
applied to 2-D gels that were processed by using the Multiphor II
system (Pharmacia). An Immobiline dry strip (pH 4 to 7) and an ExcelGel
sodium dodecyl sulfate gradient (8 to 18%) were used for the first and
second dimensions, respectively (Pharmacia). The procedure
presented in the manufacturer's manual was followed. Proteins were
visualized after staining with Coomassie brilliant blue R250.
Figure
3 shows the protein compositions
of the heat-shocked (A), optimum-temperature-grown (B), and
high-temperature-grown
cells (C). Although a number of proteins were
induced specifically
in the heat-shocked or high-temperature-grown
cells, multiple
proteins of about 35 kDa (open triangles a, b, and c)
and protein
spots of about 30 kDa (closed triangles a, b, and c) were
repeatedly
and predominantly recognized in the heat-shocked cells and
the
high-temperature-grown cells (Fig.
3). Both 35- and 30-kDa proteins
were consistently present in the optimum-temperature-grown cells
and
were increased in both the heat-shocked and the high-temperature-grown
cells. When the heat shock incubation period was increased, the
expression of 35-kDa heat shock proteins was found to be increased
(data not shown). Furthermore, the accumulation of 30-kDa proteins
in
the high-temperature-grown cells was significantly higher than
that in
the heat-shocked cells. In accordance with the degree
of induction of
these proteins, the 35-kDa heat shock proteins
and the 30-kDa
high-temperature growth-specific proteins were
designated the HSP35s
and the HGP30s, respectively. On exposure
to thermal stress, the
accumulation of a 98-kDa protein in the
hyperthermophilic archaeon ES4
and of 60-kDa heat shock proteins
in members of the order
Sulfolobales has been observed (
18,
27,
34).
However, proteins with molecular masses similar to
those of not only
such archaeal proteins but also major bacterial
heat shock proteins
such as those in the Clp family (
10), HtpG
(
4),
DnaK (
3), GroEL, and GroES (
14) were not
identified
as prominent protein components of
R. obamensis
cells under hyperthermal
conditions. The HSP35s and HGP30s in
R. obamensis were significantly
different in molecular size from
other major heat shock protein
families (
22,
25).
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FIG. 3.
2-D polyacrylamide gel electrophoresis (PAGE) analysis
of proteins from heat-shocked cells (A), optimal-temperature-grown
cells (B), and high-temperature-grown cells (C). IEF, isoelectric
focusing; SDS, sodium dodecyl sulfate.
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To identify the HSP35s and HGP30s in
R. obamensis, the
N-terminal amino acid sequences of these proteins were determined.
The
proteins in the 2-D polyacrylamide gels were transferred to
polyvinylidene difluoride membranes (Bio-Rad) by using the Multiphor
II
system, and the protein spots revealed by staining with Coomassie
brilliant blue, corresponding to the HSP35s and HGP30s, were analyzed
by Edman degradation with a 476A protein sequencer (Applied Biosystems
Inc.). The amino acid sequence
AVLEIRNLHARVEEKEILKGVNLTVNAG was
the same in
all three HSP35s, and the sequence of all three HGP30s
was
NAVDEYIPTPVRDKDKPFLMPIEDV. Multi-isoelectric heat shock proteins
were often observed in prokaryotic and eukaryotic cells based
on 2-D
polyacrylamide gel electrophoresis (
13,
20). The amino
acid
sequences of HSP35s and HGP30s were analyzed by using the
basic local
alignment search tool (
1) to estimate the degree
of
similarity to other amino acid sequences (Fig.
4). The N-terminal
amino acid sequences
of HSP35s had significant similarity to the
N-terminal sequences of the
ATP-binding subunits of bacterial
ATP-binding cassette
(ABC) transporters (Fig.
4A), while the sequences
of HGP30s were highly
similar to the internal amino acid sequences
of bacterial elongation
factor Tu (EF-Tu) (Fig.
4B). The molecular
masses of the HSP35s were
consistent with those of the ATP-binding
subunits of ABC
transporters (C subunit of the Fe-hydroximate
transporter in
E. coli and P subunits of the histidine permeases
in
E. coli and
Salmonella typhimurium) (
16,
17).
These results
implied that the HSP35s were identical polypeptides
with different
pI values and were possible components of the ABC
transporter
family in
R. obamensis. Likewise, the
sequence analysis revealed
that the HGP30s were identical proteins
having different pI values
and were derived from the EF-Tu of this
organism. The HGP30s corresponded
to the C-terminal half of EF-Tu,
resembling domains II and III
of the bacterial EF-Tu (
6,
24). This is the first report
that a high abundance of EF-Tu
lacking domain I is accumulated
in the cytoplasm under heat shock-like
or hyperthermophilic conditions.
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FIG. 4.
Similarity analysis of HSP35s (A) and HGP30s (B).
N-terminal amino acid sequences of HSP35s and HGP30s were
analyzed with the basic local alignment search tool and aligned
with closely related amino acid sequences. An asterisk or dot under the
alignment indicates identical or similar amino acids,
respectively. The amino acid sequences shown have the following
GenBank accession numbers: Cyanophora paradoxa chloroplast
ABC transporter (chlr.ABC), U30821; Porphyra
purpurea chloroplast ABC transporter (chlr.ABC), U38804; E. coli histidine transport ATP-binding protein (HisP),
D90861; Methanococcus jannaschii ABC transporter, U67462;
S. typhimurium histidine transport ATP-binding
protein (HisP), J01805; Agrobacterium tumefaciens nopaline
permease ATP-binding protein (NocP), M77785; Thermus
thermophilus EF-Tu, X06657; T. aquaticus EF-Tu, X66322;
Thermotoga maritima EF-Tu, M27479; E. coli
EF-Tu, J01690; Corynebacterium glutamicum EF-Tu,
X77034.
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In this study, it was demonstrated that the ATP-binding
subunits of the ABC transporter family and a polypeptide
homologous
to domains II and III of EF-Tu
(EF-Tu
II+III) were accumulated in heat-shocked
and high-temperature-grown
cells of
R. obamensis.
These HSP35s and HGP30s consisted of multi-isoelectric
isoforms. It has
been reported that several stress proteins also
had
isoforms with different isoelectric points, which were due
to
posttranslational modification such as phosphorylation and
adenylylation (
13,
20). In addition, the isoform
compositions
of the HSP35s of optimal-temperature-grown and
heat-shocked cells
differed. The order of the intensities of HSP35
isoforms was b
> a > c in heat-shocked cells, while it was
a > b > c in cells
grown at optimal temperatures (Fig.
3).
The result suggested that
posttranslational modification plays an
important role in the
induction and regulation of HSP35s under the heat
shock condition.
The molecular basis of the induction and regulation of these HSP35s and
HGP30s is now under investigation. First, HGP30 accumulation
mechanism
in high-temperature-grown cells and the relationship
of HGP30s to
intact EF-Tu should be clarified. To prove that the
HGP30s are formed
from the intact EF-Tu of
R. obamensis, the gene
(
tuf) for EF-Tu was analyzed by using a PCR. Part
of the
tuf gene
was amplified by a PCR with primers
having the sequences
5'-CACGTKGAYCATGGTAAAAC-3'
and
5'-TTATCWCCAGGCATWACCATYTC-3', corresponding to the
highly
conserved amino acids in the bacterial EF-Tu sequences reported
to date and nucleotide positions 58 to 77 and 1045 to 1067 in
the
E. coli tufA gene (accession no.
J01690), respectively.
About 1 kb of the PCR product was directly sequenced on both strands
by
the dideoxynucleotide chain termination method with a 373As
DNA
sequencer (Applied Biosystems Inc.). The translated amino
acid sequence
of the partial
tuf gene contained the N-terminal
amino
acid sequence of HGP30s. This indicated that the HGP30s
are
constituents of intact
R. obamensis EF-Tu. In
addition, Southern
and Northern analyses were carried out by using RNA
probes labeled
with digoxigenin (DIG)-11-UTP, corresponding to domain I
(not
the HGP30 region but nucleotide positions 58 to 550 of the
E. coli tufA gene) and domains II and III (HGP30 region,
nucleotide
positions 580 to 1067 in the
E. coli tufA gene)
of the partial
tuf gene fragment, respectively. A DIG RNA
labeling kit (Boehringer
Mannheim) was used for labeling as described
in the manufacturer's
manual. The Southern analysis indicated that
R. obamensis EF-Tu
was encoded by two copies of genes (data
not shown). In the Northern
analysis, both probes hybridized with 3.4- and 3.6-kb RNA fragments
in the optimal- and high-temperature-grown
cells, indicating that
domain I and domains II and III of the
tuf genes were transcribed
as the same transcription units
in both types of cells (Fig.
5).
Furthermore, the expression levels of the 3.4- and 3.6-kb transcription
units were much higher in the high-temperature-grown cells than
in the
optimal-temperature-grown cells (Fig.
5). These results
suggested that
the induction of HGP30s in the high-temperature-grown
cells was
preceded by induction of intact EF-Tu on the transcriptional
level, and
then HGP30s were induced and accumulated through
posttranslational
processes.
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FIG. 5.
Northern blot analysis of total RNAs from optimal- and
high-temperature-grown cells of R. obamensis. Total RNAs
were extracted from optimal- and high-temperature-grown cells with the
QuickPrep Total RNA Extraction Kit (Pharmacia). Equal amounts of RNA
(1.5 µg; lane 1, from cells grown at an optimal temperature; lane 2, from cells grown at a high temperature) were size fractionated on a
formaldehyde-denaturing agarose gel (1.0%), transferred to a
positively charged nylon membrane (Boehringer Mannheim), and hybridized
with RNA probes corresponding to domain I (A) and domains II and III
(B) of the partial tuf gene sequence, respectively.
Detection of DIG-labeled RNA hybridized with homologous RNA was carried
out with a DIG luminescence detection kit for nucleic acids (Boehringer
Mannheim). The arrows on the right indicate the 3.4- and 3.6-kb RNA
fragments that hybridized with the probes. The RNA size marker used was
from GIBCO BRL, and molecular sizes are indicated on the left.
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The proteins which accumulated under heat shock-like or
hyperthermophilic conditions have not previously been
described as
heat shock proteins despite the great number of heat
shock proteins
reported to date (
22,
25,
38). No evidence
exists that links
the enhanced thermotolerance of
R. obamensis with induction of
its HSP35s and HGP30s. However, it is
well understood that the
expression and synthesis of bacterial ABC
transporters are regulated
in response to specific growth conditions
and various cellular
functions are also regulated by the ABC
transporters (
16,
17).
These points suggest that ABC
transporters are involved in the
heat shock response in
R. obamensis and their presumed function
is the transport of
molecules into or out of the cell. Furthermore,
it has also been
pointed out that EF-Tu can participate in multiple
cellular
activities besides polypeptide chain elongation, such
as the formation
of RNA replicase (
7), interaction with adenylate
cyclase (
31), and the formation of
cytoskeleton-like filament
bundles (
5). Of these functions,
the formation of filament
bundles results from polymerization of EF-Tu
in the presence of
salts and the filaments are formed not only from
intact EF-Tu
but also from EF-Tu
II+III (
5,
12).
Recently, it has been shown that the chaperonins
in the extremely
thermophilic archaeon
S. shibatae, which are
the major heat
shock proteins and are composed of its two most
abundant proteins
(thermophilic factors 55-
and -
), form a cytoskeleton-like
filament in vitro and in vivo and that the primary function of
these
heat shock proteins is cytoskeleton formation (
37).
Therefore,
promotion of cytoskeleton formation in
high-temperature-grown
cells could be a mechanism for survival and
adaptation under hyperthermal
conditions due to the stabilization of
cell structure and immobilization
of the cell membrane.
In summary, the significant morphological changes, the enhanced
thermotolerance during hyperthermia, and the increased
abundance
of specific proteins show that a temperature-induced cellular
response occurs in the extremely thermophilic bacterium
R. obamensis.
The induced proteins, factors that could be
responsible for thermotolerance,
are different from the other heat
shock proteins reported to date.
The function of the HSP35s and
HGP30s and their role in responding
to high temperatures are the foci
of ongoing research.
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ACKNOWLEDGMENTS |
This work was supported in part by a Grant-in-Aid for Scientific
Research (no. 07556048) from the Ministry of Education, Science and
Culture of Japan and by JSPS Research Fellowships for Young Scientists
(no. 2702).
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FOOTNOTES |
*
Corresponding author. Mailing address: Deep-Sea
Microorganisms Research Group, Japan Marine Science and Technology
Center, 2-15 Natsushima-cho, Yokosuka 237, Japan. Phone:
81-468-67-3894. Fax: 81-468-66-6364. E-mail:
kent{at}jamstec.go.jp.
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J Bacteriol, May 1998, p. 2770-2774, Vol. 180, No. 10
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