Previous Article | Next Article 
Applied and Environmental Microbiology, December 1998, p. 4767-4773, Vol. 64, No. 12
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
The Mitochondrial Toxin Produced by Streptomyces
griseus Strains Isolated from an Indoor Environment Is
Valinomycin
M. A.
Andersson,1,*
R.
Mikkola,1
R. M.
Kroppenstedt,2
F. A.
Rainey,3
J.
Peltola,1
J.
Helin,4
K.
Sivonen,1 and
M.
S.
Salkinoja-Salonen1
Department of Applied Chemistry and
Microbiology,1 and
Institute of
Biotechnology,4 FIN-00014 University of
Helsinki, Finland;
Deutsche Sammlung von Mikroorganismen und
Zellkulturen, D-38124 Braunschweig,
Germany2; and
Department of Biological
Sciences, Louisiana State University, Baton Rouge, Louisiana
708033
Received 18 June 1998/Accepted 3 September 1998
 |
ABSTRACT |
Actinomycete isolates from indoor air and dust in water-damaged
schools and children's day care centers were tested for toxicity by
using boar spermatozoa as an indicator. Toxicity was detected in
extracts of four strains which caused a loss of sperm motility, and the
50% effective concentrations (EC50) were 10 to 63 ng (dry weight) ml of extended boar semen
1. The four strains were
identified as Streptomyces griseus strains by 16S ribosomal
DNA and chemotaxonomic methods. The four S. griseus strains
had similar effects on sperm cells, including loss of motility and
swelling of mitochondria, but we observed no loss of plasma membrane
integrity or depletion of cellular ATP. None of the effects was
observed with sperm cells exposed to extracts of other indoor
actinomycete isolates at concentrations of 
5,000 to 72,000 ng
ml1. The toxin was purified from all four strains and was
identified as a dodecadepsipeptide, and the fragmentation pattern
obtained by tandem mass spectrometry was identical to that of
valinomycin. Commercial valinomycin had effects in sperm cells that
were identical to the effects of the four indoor isolates of S. griseus. The EC50 of purified toxin from the S. griseus strains were 1 to 3 ng ml of extended boar
semen1, and the EC50 of commercial
valinomycin was 2 ng ml of extended boar semen1. To our
knowledge, this is the first report of the presence of ionophoric toxin
producers in an indoor environment and the first report of
valinomycin-producing strains identified as S. griseus.
| |
INTRODUCTION |
Building materials exposed to
prolonged and/or repeated moisture damage are inhabited by complex
microbial communities that include bacteria and fungi. Workers have
searched for mycotoxins, particularly satratoxin, in indoor
environments, because Stachybotrys chartarum has been
linked to damage to health in houses with moisture problems (9,
10). Bacterial toxins have received little attention as hazardous
agents in indoor environments. We searched for bacterial toxins
in indoor environments by using boar spermatozoa as indicator cells
(2). In this paper we describe Streptomyces
griseus strains that emit a toxin in indoor air and in
indoor dust. This toxin caused mitochondrial damage similar to the
previously observed damage caused by extracts obtained from a
water-damaged indoor wall in a children's day care center
(2). The toxin from Streptomyces isolates was
purified and identified, and its biochemical effects were studied.
| |
MATERIALS AND METHODS |
Media and reagents.
Nodularin was purified from
Nodularia sp. strain BY1 as described previously
(4); synthetic anatoxin A was obtained from Calbiochem-Novabiochem Corp. (La Jolla, Calif.), and enniatin was
obtained from Fluka (Buchs, Switzerland). The other commercially available reference toxins and chemicals used were obtained from the
sources described elsewhere (3). Cereulide was purified from
Bacillus cereus 4810 and F-5881 as described previously
(3). Other chemicals were of analytical quality and
were obtained from local sources.
Isolation of actinomycetes from air, dust, and building
materials.
Actinomycetes were collected from air by using an
Andersen sampler and tryptic soy agar. The plates were incubated at
22°C for 2 weeks. Strains were isolated from dust and building
materials by using resuscitation media as described previously
(2). Bacteria were cultivated for toxin production on
tryptic soy agar at 28°C.
Identification.
Whole-cell fatty acids were analyzed as
described by Nohynek et al. (17). The actinomycete isolates
were identified by using procedures described by Rainey et al.
(20) and Hain et al. (8). Genomic DNA extraction,
PCR-mediated amplification of the 16S ribosomal DNA (rDNA), and
purification of PCR products were carried out by using procedures
described by Rainey et al. (20). Purified PCR products were
sequenced with a Taq Dye-Deoxy terminator cycle sequencing
kit (Applied Biosystems, Foster City, Calif.) as recommended in the
manufacturer's protocol. An Applied Biosystems model 310 DNA genetic
analyzer was used for electrophoresis of the sequence reaction
products. Partial 16S rDNA sequences were determined by sequencing 16S
rDNA PCR products with primer 27 F. The partial 16S rDNA sequences were
aligned with sequences of members of the Actinomycetales by
using the ae2 editor (12), and pairwise similarity values
were determined.
Purification and analysis of the toxin from S. griseus strains.
Cells were harvested after 10 to 12 days
and were extracted with methanol; the methanol was evaporated, and the
residue was diluted in methanol (3). The extracts were
tested for toxic effects (inhibition of spermatozoan motility, loss of
plasma membrane integrity, decrease in cellular ATP level, swelling of
mitochondria) by using protocols described previously (3).
Methanol extracts of the S. griseus isolates were diluted
1:9 with water and injected into a Sep-pak C18 cartridge
(Waters Co., Milford, Mass.). The cartridge was eluted with
methanol-water (90:10) and with 100% methanol. The methanol extracts
were evaporated to dryness, dissolved in acetonitrile-water
(90:10) containing 0.075% trifluoroacetic acid (TFA), and
fractionated by reverse-phase high-performance liquid chromatography
(HPLC) (Smart; Pharmacia Biotech, Uppsala, Sweden) by using Sephasil
C8 SC 5 µm columns (2.1 mm [inside diameter] by
100 mm). The eluents used were water containing 0.1% TFA (eluent A) and acetonitrile containing 0.075% TFA (eluent B). A 5-min gradient from 10% (vol/vol) eluent A-90% (vol/vol) eluent B to 100%
eluent B was used. The flow rate was 100 µl/min, and detection was at
215 nm.
MS analyses.
Electrospray (ESI) mass spectra were obtained
with a model API300 triple quadrupole mass spectrometer (MS)
(Perkin-Elmer Sciex Instruments, Thornhill, Ontario, Canada). The
samples were dissolved in 50% methanol containing 5 mM ammonium
acetate and were injected into the MS with a nanoelectrospray ion
source (Protana A/S, Odense, Denmark) at a flow rate of about 30 nl/min. MS-MS spectra were obtained by colliding selected precursor
ions with nitrogen collision gas with acceleration voltages of 45 to 55 V.
Nucleotide sequence accession numbers.
The partial 16S rDNA
sequences determined in this study have been deposited in the EMBL data
library under the following accession numbers: strain 8/ppi, Y17513;
strain 10/ppi, Y17514; strain 123, Y17515; strain 157, Y17516; strain
703, Y17517; strain 147, Y17518; and strain 148, Y17519.
| |
RESULTS |
Identification of actinomycetes isolated from indoor
environment.
Strains of actinomycetes were isolated from
indoor building materials, from settled dust, and from air from
water-damaged school buildings, children's day care centers (in
Helsinki, Finland), and animal sheds (in Uusimaa County,
Finland). Twelve strains were identified by chemotaxonomic
methods and by 16S rDNA sequencing as members of the genera
Streptomyces, Nocardiopsis, and
Dietzia (Table 1).
View this table:
[in this window]
[in a new window]
|
TABLE 1.
Toxicity to boar spermatozoa of methanol-soluble
substances from actinomycetes isolated from indoor environments
|
|
Partial 16S rDNA sequences comprising around 400 nucleotides from the
5' end of the 16S RNA gene were determined for strains
8/ppi, 1/k,
2/ppi, 10/ppi, 123, 157, 703, 704, 305, 147, and 148.
The partial 16S
rDNA sequences of strains 10/ppi, 8/ppi, 1/k,
10/ppi, and 157 exhibited
showed the highest levels of similarity
(>99%) to the 16S rDNA
sequence of
S. griseus (accession no.
M76388).
The
chemotaxonomic properties of strains 2/ppi, 8/ppi, 10/ppi,
and 1/k were
diagnostic for all members of the genus
Streptomyces,
as follows: the whole-cell fatty acid composition is dominated
by iso
and anteiso fatty acids, and
LL-diaminopimelic acid is
the
diamino acid of the peptidoglycan. The strains had all of
the
conventional markers for
S. griseus, including straight
chains
of yellow spores and no melanin production.
S. griseus was the
species most frequently isolated from air in a
water-damaged school
(viable count, 60 CFU m
3) and from
dust (viable count, 50 CFU mg
1) in water-damaged schools
and children's day care
centers.
Indoor strains of S. griseus produce a
mitochondrial toxin.
Cultures of indoor actinomycete isolates were
extracted with methanol, and the extracts were tested by using boar
spermatozoa. Table 1 shows that substances extracted from three
dust-borne S. griseus strains from a children's
day care center (10/ppi, 2/ppi, and 8/ppi) and one airborne
S. griseus strain (1/k) from an elementary school
caused a loss of sperm motility at cell extract concentrations
equivalent to 10 to 60 ng of methanol-soluble solids per ml of
extended boar semen. This amount was extracted from 0.0005 to
0.002 mg of S. griseus cells (equivalent to
105 to 106 CFU). The toxicity thresholds for
the indoor Streptomyces isolates were of the same order of
magnitude as the toxicity threshold observed for the emetic toxin
(cereulide)-producing strain B. cereus 4810/72 (Table 1).
When the type strain of
S. griseus, strain DSM 40236, and
S. griseus 157 were tested similarly, they had
showed no effect
on the motility of spermatozoa at concentrations that
were up
to 1,000-fold higher (corresponding to 10
9 CFU
ml
1), indicating that toxin production was a
strain-specific characteristic.
Neither the type strain of
B. cereus (ATCC 14579) nor any of the
seven other strains of
actinomycetes that were isolated from the
same water-damaged
buildings as the toxic strains and from animal
sheds (Table
1)
affected the motility of boar spermatozoa. The
amounts of cell extract
added to the semen had no effect on the
osmolarity or pH of the
extended boar
semen.
When the sperm cells exposed to extracts prepared from
Streptomyces strains 10/ppi, 2/ppi, 8/ppi, and 1/k were
examined with
an electron microscope, we found that the extracts caused
dose-dependent
swelling of mitochondria (Fig.
1A). This indicates
that the
Streptomyces extracts contained a mitochondrial
toxin. When an extract was
fractionated by HPLC, the same HPLC fraction
caused both swelling
of mitochondria and loss of motility (Fig.
1B and
C), indicating
that the loss of motility of the sperm cells was linked
to mitochondrial
damage. No mitochondrial swelling (or loss of
motility) was observed
in sperm cells exposed to extracts of the type
strain
S. griseus DSM 40236 (Fig.
1D) or the nonemetic
strains
B. cereus ATCC 14579
T and F-3453 (data
not shown). A similar loss of motility and similar
swelling of
mitochondria were observed in sperm cells after they
were exposed
to commercial valinomycin (Fig.
1E) or to extracts
prepared from
the cereulide-producing emetic strains
B. cereus 4810/72 and
F-5881 (data not shown).
View larger version (121K):
[in this window]
[in a new window]
|
FIG. 1.
Thin sections of midpieces of boar spermatozoa exposed
to extracts of S. griseus 8/ppi (A through C), extracts
of S. griseus DSM 40236T (D), and
commercial valinomycin (E) for 7 days. (A) Midpiece of a spermatozoon
with mitochondrial damage. The frequency of swollen mitochondria in the
spermatozoan midpiece was >60% after exposure to 20 µg (dry weight)
of strain 8/ppi crude extract per ml. After exposure to 2 µg
ml1 the frequency of swollen mitochondria was <20%
(data not shown). (B) Thin section of the midpiece of a boar
spermatozoon exposed to a toxic strain 8/ppi HPLC fraction, showing
swollen mitochondria with disrupted outer membranes. (C) Midpiece of a
spermatozoon exposed to a nontoxic strain 8/ppi HPLC fraction. (D)
Section of a midpiece exposed to a similarly prepared S. griseus DSM 40236T extract (20 µg [dry weight] per
ml of extended boar semen). (E) Midpiece after exposure to 200 ng of
commercial valinomycin ml1. Bars = 200 nm.
|
|
The spermatozoon-paralyzing agent in the extracts of cultures of
S. griseus 2/ppi, 8/ppi 10/ppi, and 1/k was not
sensitive
to heating at 100°C (20 min), to treatment with acid (pH 2 HCl,
30 min) or alkali (pH 12, NaOH, 30 min), or to the action of
pronase
(Sigma) (100 µg ml
1, pH 7, 3 h, 37°C).
This toxic agent could pass through microconcentrator
membrane filters
with nominal cutoffs of 100,000 and 10,000 g
mol
1 as a
methanol extract but not as an extract in water or dimethyl
sulfoxide
(DMSO). Thus, the sperm cell-paralyzing agent extracted
from the indoor
S. griseus strains was heat stable, nonpolar,
and
resistant to inactivation by heat, by extreme pH, or by protease
and
had an apparent molecular size of less than 10,000 g
mol
1. In these respects it behaved like the extract
prepared from
the emetic strain
B. cereus 4810/72.
Purification and identification of the toxin from S. griseus 2/ppi, 8/ppi, 10/ppi, and 1/k.
HPLC fractions which
contained the agent toxic to sperm were collected (Fig.
2A). The fractions representing a single
peak in strains 2/ppi, 8/ppi, 10/ppi, and 1/k were evaporated in a stream of N2, dissolved in methanol, and analyzed by ESI
MS. Figure 2B shows the ESI MS-MS spectrum obtained for the
ammonium adduct of the purified toxin from S. griseus
8/ppi (ion m/z 1,128.84). Figure 2C shows the spectrum
obtained for the ammonium adduct valinomycin (ion m/z
1,128.64). The first fragment lost from the S. griseus 8/ppi toxin was ammonia, and the result was a
protonated molecular ion of m/z 1,111.84 (Fig. 2B).
This ion was similar to the protonated molecular ion m/z
1,111.64, which was obtained from commercial valinomycin (Sigma) (Fig.
2C). The assignments of the fragment ions observed are shown in Table
2. The mass values for all fragment
losses observed with the toxin from S. griseus 8/ppi
and commercial valinomycin (Sigma) were compared to the fragmentation
pattern expected based on the structure of valinomycin, and they
matched within 0.34 and 0.23 mass unit, respectively. The mass values
for all fragment losses observed with the S. griseus
8/ppi toxin matched within 0.31 mass unit the mass values observed with
the valinomycin standard. The ESI MS-MS spectra of the toxins purified
from S. griseus 2/ppi, 10/ppi, and 1/k (data not shown)
were identical to the spectra of the S. griseus 8/ppi
toxin and to the spectra of the valinomycin standard. These data
indicate that the methanol-extractable toxins of S. griseus 2/ppi, 8/ppi, 10/ppi, and 1/k were identical to
valinomycin, a cyclic dodecadepsipeptide. The yields of valinomycin
from 10- to 12-day-old cultures of the S. griseus
strains were 600 to 1,400 ng mg (wet weight) of cells1,
as determined by HPLC in which commercial valinomycin was used for
quantitation.
View larger version (24K):
[in this window]
[in a new window]
|
FIG. 2.
HPLC fractionation and ESI MS-MS fragmentation of the
toxin from S. griseus 8/ppi and commercial valinomycin.
(A) HPLC elution profiles of the extract from S. griseus 8/ppi and commercial valinomycin ESI-MS-MS fragmentation
patterns of an ammonium adduct of the toxin purified from S. griseus 8/ppi (ion m/z 1,128.84) (B) and of an ammonium
adduct of commercial valinomycin (ion m/z 1,128.64). (C)
Samples were dissolved in 50% methanol containing ammonium acetate for
the MS analysis. The peak numbers correspond to the fragment ions
assigned in Table 2. The peaks marked with asterisks represent loss of
water.
|
|
View this table:
[in this window]
[in a new window]
|
TABLE 2.
Fragment ions and fragment losses in the MS-MS spectra of
the toxin from S. griseus 8/ppi and
commercial valinomycin
|
|
Biological properties of purified sperm-toxic agent from
S. griseus 2/ppi, 8/ppi, 10/ppi, and 1/k compared to
the biological properties of other toxins and chemicals.
Table
3 shows the toxicity thresholds for the
S. griseus sperm toxin, valinomycin, extracted from
strains 2/ppi, 8/ppi, 10/ppi, and 1/k with boar spermatozoa, and for
selected microbial toxins and chemicals. The toxicity thresholds for
valinomycin purified from four strains of S. griseus
were between 1 and 3.2 ng ml of extended boar semen1. The
following seven preparations were toxic to sperm cells: purified toxins
from S. griseus 10/ppi, 8/ppi, 2ppi, and 1/k, cereulide
purified from B. cereus 4810/72 and F5881, and commercially obtained valinomycin and gramicidin. Valinomycin and cereulide caused a
loss of sperm motility at concentrations of 
3 ng ml1
and caused mitochondria to swell at concentrations of <400 ng ml1 but did not deplete ATP in the cells at
concentrations up to 12,500 ng ml1. Gramicidin (<3 ng
ml1) caused a loss of motility. Calcimycin A 23187 caused
a loss of motility at a concentration of 32 ng ml1 and
depleted ATP at a concentration of 125 ng ml1 but caused
no visible morphological damage to sperm cells even at a concentration
of 2,000 ng ml1. Enniatin inhibited motility at a
concentration of 300 ng ml1 but did not cause
mitochondria to swell at concentrations up to 5,000 ng
ml1. The sperm cells were not sensitive to nodularin and
to commercial preparations of anatoxin a, ionomycin, surfactin,
polymyxin B, and 2,4-dinitrophenol; the 50% effective concentrations
(EC50) of these compounds for the spermatozoan vitality
parameters ranged from 100 to >50,000 ng ml1 (Table 3).
N,N-Dihexylcarbodiimide caused mitochondria to swell at a
concentration of 1,000 ng ml1. In conclusion, the
extracts prepared from S. griseus 10/ppi, 8/ppi, 2/ppi,
and 1/k eliminated motility and caused mitochondria of sperm cells to
swell, as did cereulide from emetic B. cereus strains and
valinomycin, while the other compounds tested had no effect or had an
effect only at dosages that were 1,000- to 10,000-fold higher.
| |
DISCUSSION |
We found that S. griseus isolates obtained from
dust and air in water-damaged buildings produced valinomycin. We showed
previously that extracts from water-damaged indoor building materials
paralyzed sperm and caused mitochondria to swell (2).
Identical effects were observed with pure cultures of S. griseus strains, as well as commercially obtained
valinomycin. Valinomycin-producing cultures were readily isolated
from dust and air from water-damaged buildings.
The cultures of S. griseus 8/ppi, 2/ppi, 10/ppi, and
1/k contained about 1 µg of valinomycin per mg (wet weight) of cells. The airborne S. griseus viable count in the
building was 60 CFU m3, and the dust viable count was 50 CFU mg1. Viable counting of airborne and
dust-borne bacteria is known to underestimate the cell count by factors
of 1,000 to 10,000 (14, 15, 18). Viable as well as nonviable
Streptomycetes spores may remain airborne due to their
small size and great hydrophobicity (16). Therefore, the
actual airborne load of S. griseus biomass in the
water-damaged school and children's day care centers may have reached
a level of 105 cells m3, which is equivalent
to 0.1 ng of valinomycin m3.
Valinomycin is a potassium ionophore (7). It eliminated
progressive and rapid motility in exposed boar spermatozoa but did not
affect plasma membrane integrity or the intracellular levels of ATP,
indicating that ATP production by glycolysis continued to be
active. Swelling of the inner mitochondrial membrane was observed in
spermatozoa paralyzed by valinomycin; this is similar to effects
observed with another toxic dodecadepsipeptide, cereulide, isolated
from emetic food-poisoning outbreaks (3). No mitochondrial swelling was observed in sperm cells paralyzed by gramicidin, a
membrane channel-forming linear homopeptide protonophore
(7).
Depsipeptide toxins acting as ionophores and creating ion channels
across bacterial or mitochondrial membranes (5, 7) are known
to be produced by many bacteria and fungi. The significance of such
toxins in the environment is not known due to the lack of a suitable
bioassay for detection in environmental samples. Boar spermatozoa
proved to be sensitive indicator cells as they lost motility when they
were exposed to extremely low doses (1 ng ml1) of
valinomycin, gramicidin, and cereulide. The low sterol content of the
boar spermatozoan plasma membrane makes these cells permeable, whereas
the spermatozoa of other domestic animals and humans, which have higher
amounts of sterols in the plasma membrane, are less sensitive to
ionophores (5, 19). Boar spermatozoa are ineffective under
anoxic conditions and exhibit only flickering motility in the absence
of oxidative phosphorylation (13). Boar spermatozoan
motility, therefore, is a sensitive indicator for agents that affect
oxidative phosphorylation.
Disrupted mitochondrial physiology and swelling and ongoing
cytosolic ATP synthesis have been shown to trigger both apoptotic and
necrotic processes (23), indicating that exposure to
mitochondrial toxins may be a severe health hazard. Cereulide, a
depsipeptide ionophore produced by emetic strains of B. cereus, has been shown to cause fatal food poisoning and
mitochondrial damage in inner organs when it is ingested (1, 11,
22). Members of the genus Streptomyces have been
isolated frequently from water-damaged buildings (21). It is
known that valinomycin is produced by Streptomyces
fulvissimus, a species that is not related to S. griseus as determined by 16S rDNA sequence comparisons
(20a). Valinomycin production is thus a strain-specific
characteristic, not a species-specific characteristic, that may be
exhibited by many other Streptomyces species found in indoor
air and dust. Exposure to microbially generated mitochondrial toxins
that are inhaled may pose a risk to organs that are rich in
mitochondria and depend on oxidative phosphorylation (e.g., the brain,
heart, and kidneys). Acute renal failure due to inhalation of
mycotoxins has been reported (6).
The S. griseus toxin, which is identical to
valinomycin, was extremely stable under extreme environmental
conditions. This toxin may accumulate for long periods of time
when building materials are exposed to repeated water damage. To
our knowledge, this is the first report of isolation of an ionophoric
toxin from indoor air or dust in water-damaged buildings. This is
also the first report of valinomycin-producing strains that are
identified as S. griseus.
| |
ACKNOWLEDGMENTS |
This work was financially supported by grants from the Foundation
of Work Environment (Finland), the Centre of Excellence Fund of the
University of Helsinki, the Technology Development Center of Finland,
and the Academy of Finland.
We thank the Artificial Insemination Center (AI Cooperative, Kaarina,
Finland) and Magnus Andersson (Department of Animal Reproduction,
Helsinki University) for providing the boar semen. We thank Tuire Koro
and Mervi Lindman for preparing thin sections. Equipment at the
laboratory for electron microscopy of the Helsinki University Biocenter
was at our disposal.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Applied Chemistry and Microbiology, POB 56, Helsinki University FIN
000140, Finland. Phone: 358 9 70859339. Fax: 358 9 7085322. E-mail:
Maria.A.Andersson{at}helsinki.fi.
| |
REFERENCES |
| 1.
|
Agata, N.,
M. Ohta,
M. Masashi, and M. Isobe.
1995.
A novel dodecadepsipeptide, cereulide, is an emetic toxin of Bacillus cereus.
FEMS Microbiol. Lett.
129:17-20[Medline].
|
| 2.
|
Andersson, M. A.,
M. Nikulin,
U. Köljalg,
M. C. Andersson,
F. A. Rainey,
K. Reijula,
E.-L. Hintikka, and M. Salkinoja-Salonen.
1997.
Bacteria, molds, and toxins in water-damaged building materials.
Appl. Environ. Microbiol.
63:387-397[Abstract].
|
| 3.
|
Andersson, M. A.,
R. Mikkola,
J. Helin,
M. C. Andersson, and M. Salkinoja-Salonen.
1998.
A novel sensitive bioassay for detection of Bacillus cereus emetic toxin and related depsipeptide ionophores.
Appl. Environ. Microbiol.
64:1338-1343[Abstract/Free Full Text].
|
| 4.
|
Annila, A.,
J. Lehtimäki,
K. Mattila,
J. Eriksson,
K. Sivonen,
T. Rantala, and T. Drakenberg.
1996.
Solution structure of nodularin, an inhibitor of serine/threonine-specific protein phosphatases.
J. Biol. Chem.
271:16695-16702[Abstract/Free Full Text].
|
| 5.
|
Booth, I.
1988.
Bacterial transport energetics and mechanisms, p. 377-428.
In
C. Anthony (ed.), Bacterial energy transduction. Academic Press, London, United Kingdom.
|
| 6.
|
Di Paolo, N.,
A. Guarnieri,
F. Loi,
G. Sacchi,
A. Mangiarotti, and M. Di Paolo.
1993.
Acute renal failure from inhalation of mycotoxins.
Nephron
64:621-625[Medline].
|
| 7.
|
Gräfe, U.
1992.
Biochemie der Antibiotika: Struktur-Biosynthese-Wirkmechanismus, p. 167.
and 219-318. Spectrum Akademischer Verlag GmbH, Heidelberg, Germany.
|
| 8.
|
Hain, T.,
N. Ward-Rainey,
R. Kroppenstedt,
E. Stackebrandt, and F. Rainey.
1997.
Discrimination of Streptomyces albidoflavus strains based on the size and number of 16S-23S ribosomal DNA intergenic spacers.
Int. J. Syst. Bacteriol.
47:202-206[Abstract/Free Full Text].
|
| 9.
|
Hendry, K., and E. Cole.
1993.
A review of mycotoxins in indoor air.
J. Toxicol. Environ. Health
38:183-189[Medline].
|
| 10.
|
Johanning, E.,
D. Biagini,
D. Hull,
P. Morey,
P. Jarvis, and P. Landsbergis.
1996.
Health and immunology study following exposure to toxigenic fungi (Stachybotrys chartarum) in water-damaged office environment.
Int. Arch. Occup. Environ. Health
68:207-218[Medline].
|
| 11.
|
Mahler, H.,
A. Pasi,
J. Kramer,
P. Schulte,
A. Scoging,
W. Baer, and S. Kraehenbuehl.
1997.
Fulminant liver failure in association with the emetic toxin of Bacillus cereus.
N. Engl. J. Med.
336:1143-1148.
|
| 12.
|
Maidak, B.,
N. Larsen,
M. McCaughey,
R. Overbeek,
G. Olsen,
K. Fogel,
J. Blandy, and C. Woese.
1994.
The Ribosomal Database Project.
Nucleic Acid Res.
22:3485-3487[Abstract/Free Full Text].
|
| 13.
|
Mann, T., and C. Lutwak-Mann.
1982.
Male reproductive function and semen, p. 196-197.
Springer Verlag, Heidelberg, Germany.
|
| 14.
|
Marthi, B.
1994.
Resuscitation of microbial aerosols, p. 192-225.
In
B. Lightheart, and A. Mohr (ed.), Atmospheric microbial aerosols. Chapman & Hall, New York, N.Y.
|
| 15.
|
McFeters, G.,
F. Yu,
B. Pyle, and P. Stewart.
1995.
Physiological assessment of bacteria using fluorochromes.
J. Microbiol. Methods
21:1-13.
[Medline] |
| 16.
|
Mozer, N., and P. Rouxhet.
1987.
Methods for measuring hydrophobicity of microorganisms.
J. Microbiol. Methods
6:99-112.
|
| 17.
|
Nohynek, L.,
M. Häggblom,
N. Palleroni,
K. Kronquist,
E.-L. Nurmiaho-Lassila, and M. Salkinoja-Salonen.
1993.
Characterization of Mycobacterium fortuitum strain capable of degrading polychlorinated phenolic compounds.
Syst. Appl. Microbiol.
16:126-134.
|
| 18.
|
Palmgren, U.,
G. Ström,
G. Blomquist, and P. Malmberg.
1986.
Collection of airborne microorganisms on Nuclepore filters, estimation and analysis CAMNEA method.
J. Appl. Microbiol.
61:401-406.
|
| 19.
|
Paulenz, H.
1993.
Spermiemembranens struktur og funksjon I relasjon til kuldesjokk.
Nor. Veterinaertidskr.
105:1135-1142.
|
| 20.
|
Rainey, F.,
N. Ward-Rainey,
R. Kroppenstedt, and E. Stackebrandt.
1996.
The genus Nocardiopsis represent a phylogenetically coherent taxon and a distinct actinomycete lineage: proposal of Norcardiopsaceae fam. nov.
Int. J. Syst. Bacteriol.
46:1088-1092[Abstract/Free Full Text].
|
| 20a.
| Rainey, F. A. Unpublished data.
|
| 21.
|
Räty, K.,
O. Raatikainen,
J. Holmalahti,
A. von Wright,
S. Joki,
A. Pitkänen,
V. Saano,
A. Hyvärinen,
A. Nevalainen, and I. Buti.
1996.
Biological activities of actinomycetes and fungi isolated from the indoor air of problem houses.
Int. Biodeter. Biodeter.
1996:134-154.
|
| 22.
|
Sakurai, N.,
K. Koike,
Y. Irie, and H. Hayashi.
1994.
The rice culture filtrate of Bacillus cereus isolated from emetic type food poisoning causes mitochondrial swelling in a HEp-2 cell.
Microbiol. Immunol.
38:337-343[Medline].
|
| 23.
|
Vander Heiden, M.,
N. Chandel,
E. Williamson,
P. Schumacker, and C. Thompson.
1997.
Bcl-XL regulates the membrane potential and volume homeostasis of mitochondria.
Cell
91:627-637[Medline].
|
Applied and Environmental Microbiology, December 1998, p. 4767-4773, Vol. 64, No. 12
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Hong, J. H., Hong, J. Y., Park, B., Lee, S.-I., Seo, J. T., Kim, K.-E., Sohn, M. H., Shin, D. M.
(2008). Chitinase Activates Protease-Activated Receptor-2 in Human Airway Epithelial Cells. Am. J. Respir. Cell Mol. Bio.
39: 530-535
[Abstract]
[Full Text]
-
Peltola, J., Ritieni, A., Mikkola, R., Grigoriev, P. A., Pocsfalvi, G., Andersson, M. A., Salkinoja-Salonen, M. S.
(2004). Biological Effects of Trichoderma harzianum Peptaibols on Mammalian Cells. Appl. Environ. Microbiol.
70: 4996-5004
[Abstract]
[Full Text]
-
Peltola, J. S. P., Andersson, M. A., Kampfer, P., Auling, G., Kroppenstedt, R. M., Busse, H.-J., Salkinoja-Salonen, M. S., Rainey, F. A.
(2001). Isolation of Toxigenic Nocardiopsis Strains from Indoor Environments and Description of Two New Nocardiopsis Species, N. exhalans sp. nov. and N. umidischolae sp. nov.. Appl. Environ. Microbiol.
67: 4293-4304
[Abstract]
[Full Text]
-
Peltola, J., Andersson, M. A., Haahtela, T., Mussalo-Rauhamaa, H., Rainey, F. A., Kroppenstedt, R. M., Samson, R. A., Salkinoja-Salonen, M. S.
(2001). Toxic-Metabolite-Producing Bacteria and Fungus in an Indoor Environment. Appl. Environ. Microbiol.
67: 3269-3274
[Abstract]
[Full Text]
-
Pidoux, O., Argenson, J.-N., Jacomo, V., Drancourt, M.
(2001). Molecular Identification of a Dietzia maris Hip Prosthesis Infection Isolate. J. Clin. Microbiol.
39: 2634-2636
[Abstract]
[Full Text]
-
Zahn, J.A., Hatfield, J.L., Laird, D.A., Hart, T.T., Do, Y.S., DiSpirito, A.A.
(2001). Functional Classification of Swine Manure Management Systems Based on Effluent and Gas Emission Characteristics. J. Environ. Qual.
30: 635-647
[Abstract]
[Full Text]
-
Paananen, A., Mikkola, R., Sareneva, T., Matikainen, S., Andersson, M., Julkunen, I., Salkinoja-Salonen, M. S., Timonen, T.
(2000). Inhibition of Human NK Cell Function by Valinomycin, a Toxin from Streptomyces griseus in Indoor Air. Infect. Immun.
68: 165-169
[Abstract]
[Full Text]
Top
Abstract
Introduction
