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The Mycology Group, BioCentrum-DTU, Søltofts Plads, Building 221, Technical University of Denmark, DK-2800 Kgs. Lyngby, Denmark
Kristian F. Nielsen
The Mycology Group, BioCentrum-DTU, Søltofts Plads, Building 221, Technical University of Denmark, DK-2800 Kgs. Lyngby, Denmark Energy and Indoor Climate Division, Danish Research Institute, Dr. Neergaardsvej 15, DK-2970, Hørsholm, Denmark
Bruce B. Jarvis
Department of Chemistry and Biochemistry and the Joint Institute for Food Safety and Applied Nutrition (JIFSAN), University of Maryland, College Park, Maryland 20742, USA
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Stachybotrys was found to be associated with idiopathic pulmonary hemorrhage in infants in Cleveland, Ohio. Since that time, considerable effort has been put into finding the toxic components responsible for the disease. The name Stachybotrys chartarum has been applied to most of these isolates, but inconsistent toxicity results and taxonomic confusion prompted the present study. In this study, 122 Stachybotrys isolates, mainly from water-damaged buildings, were characterized and identified by combining three different approaches: morphology, colony characteristics, and metabolite production. Two different Stachybotrys taxa, S. chartarum and one undescribed species, were found in water-damaged buildings regardless of whether the buildings were in Denmark, Finland, or the USA. Furthermore, two chemotypes could be distinguished in S. chartarum. One chemotype produced atranones, whereas the other was a macrocyclic trichothecene-producer. The second undescribed taxon produced atranones and could be differentiated from S. chartarum by its growth characteristics and pigment production. Our results correlate with different inflammatory and toxicological properties reported for these same isolates and show that the three taxa/chemotypes should be treated separately. The co-occurrence of these three taxa/chemotypes in water-damaged buildings explains the inconsistent results in the literature concerning toxicity of Stachybotrys isolated from that environment.
Key words: Atranones, colony diameter, identification, macrocyclic trichothecenes, pigment production, Stachybotrys chartarum
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Gravesen et al 1999
), and Stachybotrys has become the focus of attention after reports of its association with idiopathic pulmonary hemorrhage (IPH) in infants in Cleveland, Ohio (Dearborn et al 1999
, Vesper et al 2000b
). Stachybotryo-toxicoses have long been known in agriculture when wet, Stachybotrys-infected hay was consumed by farm animals (Forgacs and Carll 1962
). The strong cellulolytic ability of species of Stachybotrys (Udagawa 1984
) also allows it to grow on water-damaged building materials such as gypsum board, wallpaper and insulation (Gravesen et al 1999
). Macrocyclic trichothecenes (e.g., satratoxins, roridins and verrucarins) seem to be the causative components of toxicoses for farm animals eating contaminated hay (Jarvis et al 1986
). Considerable effort is now being put into finding the toxic components associated with IPH.
In addition to the macrocyclic trichothecenes, species of Stachybotrys are able to produce a number of other components or secondary metabolites: simple trichothecenes, such as trichodermol and trichodermol acetate (trichodermin), (Nielsen et al 1998a
, Hinkley and Jarvis 2000
); atranones, including their dolabellane precursors (Hinkley et al 2000
); spirocyclic drimanes (Ayer and Miao 1993
, Jarvis et al 1995
); trichoverroids (Croft et al 1986
) and the hemolytic protein stachylysin (Vesper et al 2001
). Some of these metabolites can cause skin irritation (Gravesen et al 1994
) or have immunosuppressant effects (Fung et al 1998
). Others are cytotoxic and can induce inflammatory responses (Routsalainen et al 1998
) and may be a cause of IPH (Vesper et al 2001
). Both in vitro and in vivo studies have revealed novel components that induce inflammation (Routsalainen et al 1998
), altered surfactant production in lung tissue (Mason et al 2001
), and membrane damage (Peltola et al 1999
). Finally, it has been shown that Stachybotrys can produce some of its metabolites during growth on water-damaged building materials in the laboratory (Croft et al 1986
, Nielsen et al 1998a,b
, Vesper et al 2000b
).
Because Stachybotrys is considered to be responsible for toxicoses in humans (Flannigan and Miller 1994
), it is of great importance that this fungus is detected (Andersen and Nissen 2000
) and identified quickly and correctly. The list of synonyms for S. chartarum (Ehrenb. ex Link) Hughes, however, is long and the inconsistent use of S. chartarum and the synonyms, S. atra Corda and S. alternans Bon., has contributed to the taxonomic confusion.
In addition to morphology, other approaches have been applied in order to facilitate correct identification of fungi. The production of different metabolites in different species has been used as a means of species characterization and identification in Aspergillus, Fusarium and Penicillium (Frisvad and Filtenborg 1990
, Frisvad et al 1998
) and Alternaria (Andersen et al 2001
), but only few papers dealing with species specific metabolites produced by Stachybotrys exist (El-Maghraby et al 1991
). Physiological criteria, such as growth characteristics on different media and at different water activities and temperatures, have also been used to aid identification of species in Penicillium (Pitt 1980
) and Alternaria (Andersen et al 2001
), but such approaches have never been used systematically in the characterization and identification of Stachybotrys. Jong and Davis (1976)
did, however, record pigmentation and colony diameter.
The purpose of this study was to characterize Stachybotrys isolates from water-damaged buildings by combining morphology and growth characteristics with metabolite production in order to determine which taxa are present and to facilitate future identification efforts. The study included 28 Stachybotrys isolates from the USA, 30 from Finland, and 15 from Denmark, all isolated from water-damaged buildings. An additional 49 Stachybotrys isolates from substrata other than building material and from culture collections were included.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), Czapek yeast extract agar (CYA) (Samson et al 2000
), Potato sucrose agar (PSA) (Samson et al 2000
), Sigma yeast extract sucrose agar (SYES) (Filtenborg et al 1990
), V8 juice agar (V8) (Simmons 1992
) and Cornmeal agar (CMA) (DIFCO Manual 1969
). The inoculated plates were put in perforated plastic bags and incubated in darkness at 25 C for 7 d.
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. The isolates were mounted in lactophenol using tape preparations (Butler and Mann 1959
) and examined at 400 x and 1000 x magnification. After examination, all isolates on PSA were re-incubated for 7 d in darkness at 25 C before extraction. Statistical data analysis – A data matrix, consisting of 78 objects (Stachybotrys isolates) and 10 variables (colony diameters and pigmentation on the five media), was constructed. The matrix was standardized (the variable was divided by the maximum value of each variable) and analyzed using Manhattan and UPGMA in NTSYS (Applied Biostatistics Inc., New York. Version 2.02j for Windows).
Chemicals and metabolite standards –
All chemicals used were either analytical or HPLC grade. Heptafluorobuturylimidazol (HFBI) and verrucarol (VER) were obtained from Sigma (St. Louis, Missouri, USA) and 1,12-dodecanediol was obtained from Fluka (Buchs, Switzerland). Trichodermin was provided by Dr. Jytte Hansen, Løvens Kemiske Fabrik A/S (Ballerup, Denmark) and trichodermol was derived by hydrolyzing trichodermin. Standards of satratoxins H, G and iso-F, roridin E, verrucarins B and J, atranones A to H, griseofulvin, dechlorofulvin and iso-dechlorogriseofulvin were available from previous studies in the laboratory of BBJ. Other compounds were compared by their retention indices and UV-spectra to the Mycology Group database containing about 450 fungal secondary metabolites (Frisvad and Thrane 1987
, Smedsgaard 1997
).
Preparation of extracts –
From 14-d colonies on PSA, ten agar plugs (6 mm in diam) were cut from each isolate and transferred to a 2 mL vial. 1.5 mL methanol was then added and the vials were left overnight. The next day the methanol was transferred to a clean 2 mL vial and evaporated to dryness in a rotary vacuum concentrator (Christ, Gefriertrocknungsanlagen GmbH, Germany) at 1 mbar, 1300 rpm and 25 C. Polyethylene imine (PEI) silica columns (Jarvis 1992
) were prepared in 2-mL disposable syringes by packing 1 mL PEI tightly between 2 discs of porous polyethylene filter support material. The columns were preconditioned with 6 mL methanol followed by 6 mL dichloromethane. The dried methanol extract was re-dissolved in 1 mL dichloromethane, loaded onto the column and eluded with 10 mL dichloromethane. The extracts were evaporated to dryness and re-dissolved in 100 µL methanol and filtered through a 0.45 µm syringe filter (Titan 44513-PL, SRI, Eaton town, NJ, USA) into clean 2 mL vials.
HPLC analysis –
Extracts were analyzed on an HP 1090 Series II HPLC equipped with a diode array detector and a C18 column using water-acetonitrile gradient system as described by Smedsgaard (1997)
. The 260 nm signal was used as the detection wavelength, and retention times and UV-spectra were compared with reference standards of trichothecenes, atranones and griseofulvins and with standards from the Mycology Group metabolite database.
GC-MS-MS analysis –
After HPLC analysis the vials with extract were prepared for GC analysis. 100 µL internal standard (0.8 µg 1,12-dodecanediol/mL methanol) was added to each vial and then evaporated to dryness. The samples were redissolved in 200 µL 0.2 M NaOH in methanol and hydrolyzed overnight. The parent trichothecene alcohols, trichodermol (partly originating from trichodermin) and verrucarol (originating from macrocyclic trichothecenes) were derivatized to their heptafluorobuturyl esters and detected using simultaneous GC-MS and GC-MS-MS analysis on a GCQ (Finnigan Corporation, Austin, Texas, USA) as described by Nielsen and Thrane (2001)
.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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and the results are shown in Table I
. All of the 18 cultures from various culture collections that arrived as S. albipes, S. bisbyi, S. cylindrospora, S. dichroa, S. microspora, S. nephrospora, S. oenanthes, S. parvispora, S. theobromae and S. nilagirica fit the respective descriptions by Jong and Davis (1976)
and Subramanian (1957)
well.
Of the 17 cultures from culture collections that had been deposited as S. chartarum, 14 fit the description of S. chartarum by Jong and Davis (1976)
with branched conidiophores and ellipsoidal conidia with a banded or ridged surface. Of the 88 isolates originating from Danish, Finnish, and American building-related material, 70 were identified as S. chartarum. The three remaining cultures from culture collections (ba 173 [= IHEM 2248], IBT 9754 [= IHEM 9905] and IBT 9767 [= NRRL 29940 = QM 94d]), were morphologically similar to each other and had the same distinct appearance as the remaining 18 isolates from building materials. These 21 isolates, labeled "Stachybotrys sp. Group A" (Group A) in Table I
, did not fit any described species of Stachybotrys treated by Subramanian (1957)
, Barron (1961)
, Ellis (1971, 1976)
, Jong and Davis (1976)
, Domsch et al (1980)
, Dorai and Vittal (1986)
or by McKenzie (1991)
.
The conidiophores and phialides of these Group A isolates looked similar on CMA to those of S. chartarum, while the conidia resembled those of S. albipes. The Group A isolates had dark, branched, tuberculate conidiophores and obovate phialides as compared to the S. albipes isolates that had simple, smooth, and hyaline conidiophores and ellipsoidal phialides. The conidia of the Group A isolates were ovate (9 x 5 µm) with a smooth surface and a scar at the base, in contrast to the S. chartarum isolates that had ellipsoidal conidia (11 x 4 µm) with a rough surface.
Of the 28 Stachybotrys isolates from Cleveland, Ohio, 22 isolates were identified as S. chartarum and six as Group A, while 28 isolates from Finnish building materials were identified as S. chartarum and only two as Group A. Eleven of the 15 isolates from Danish buildings were S. chartarum and four were Group A.
Metabolite production –
Initially, crude extracts of 40 American and Finnish isolates were made from cultures grown on each of the five media (ALK, CYA, PSA, SYES, and V8) and analyzed by HPLC-DAD with no prior cleanup. The spirocyclic drimanes overshadowed all other compounds produced in the extracts (Compare HPLC chromatograms in Fig. 1A and 1B ), and no correlation between the two morphologically distinguishable groups and drimane production was found. However, the Group A isolates generally produced fewer of the drimane components resembling the ‘Mer-NF5003’ (Fig. 1A
) described by Kaneto et al (1994)
albeit in much higher quantities than the S. chartarum isolates. This type of drimane has not been detected in rice cultures previously. On ALK, lactones and lactams (also spirocyclic drimanes) were the most dominant components. The S. chartarum isolates that were able to produce macrocyclic trichothecenes did so consistently on all five media.
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Ten of the 22 S. chartarum isolates from Cleveland and 12 of 28 S. chartarum from Finland produced macrocyclic trichothecenes. Only three of 11 Danish S. chartarum isolates produced these compounds.
Growth characterization – Colony appearance varied in both size and color among the 12 different Stachybotrys species or taxa, but was stable among isolates within each species or taxa. The media ALK, SYES, and V8 supported only sparse pigment production for most of the 122 Stachybotrys isolates. Only S. chartarum and Group A produced extracellular pigment on both CYA and PSA, as did the single isolate of S. microspora, which produced a greenish yellow pigment. Table II lists the colors of the pigments and the mean colony diameters (±twice the standard deviation) for all isolates identified as either S. chartarum or Group A. There was no obvious difference in either pigmentation or size of colonies between the S. chartarum isolates that produced macrocyclic trichothecenes (M) and those that produces atranones (A). In general, the atranone-producing isolates had slightly larger colonies and did not produce the yellow pigment on CYA. The production of yellow pigment by the two S. chartarum groups was not consistent, in contrast to pigment production by Stachybotrys sp. Group A isolates. All 21 Group A isolates produced a halo of jade green extracellular pigment around each colony on CYA and PSA. Their colony diameters were markedly smaller that those of the S. chartarum isolates (Table II ).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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A preliminary RAPD-PCR experiment showed that two Stachybotrys sp. Group A isolates (IBT 9299 and IBT 9467) had identical RAPD profiles that were different from the profiles of five S. chartarum isolates (results not shown). Among the S. chartarum isolates in this experiment there were no differences between RAPD-profiles of macrocyclic trichothecene-producing isolates (IBT 9631 and IBT 9632) and atranone-producing isolates (IBT 9292, IBT 9633 and IBT 9634). They could, however, be distinguished by AFLP analysis (results not shown).The two chemotypes in S. chartarum, the atranone producers and the macrocyclic trichothecene producers, need to be examined in order to establish if there is more subtle morphological evidence to suggest that they should be two separate sibling species.
Three Stachybotrys isolates [IBT 9768 (= ATCC 16026 = NRRL 29942 = NC-1), IBT 9769 (= ATCC 26303 = NRRL 29941 = NC-4) and IBT 9767 (= ATCC 11695 = NRRL 29940)] that had been included in the study of Jong and Davis (1976)
as S. chartarum were also examined in this study. Two of these isolates, IBT 9768 and IBT 9769, produced rough-surfaced conidia when mature and were identified as S. chartarum, while the third isolate, IBT 9767, produced smooth conidia regardless of age and was identified as Stachybotrys sp. Group A. Stachybotrys atra was depicted as having smooth conidia by Corda (as reproduced in Bisby 1943
), but based on three new cultures Bisby (1943)
re-described S. atra as having both smooth and rough conidia. The three isolates used by Bisby are not available and no neotype was designated. Accepting Bisby and Hughes' arguments, Jong and Davis (1976
: 435) describe the mature conidia of S. chartarum as "...dark olive gray, more or less opaque, smooth-walled or showing banded or ridged,..." and later (1976: 439) write that "The distinguishing feature of this species is the mature phialoconidia showing a ridged or banded surface and their size.". It may be incorrect that S. atra Corda is synonymous with S. chartarum (Ehrenberg) S. (Ehrenb. ex Link) Hughes. The question of whether Stachybotrys sp. Group A is a new, undescribed species or actually S. atra as Corda described it cannot be resolved until neotypes of the two species have been designated.
Ten of the 16 Stachybotrys isolates from Cleveland, analyzed by both Jarvis et al (1998)
and Vesper et al (1999, 2000a)
, were examined in this study (marked with 
in Table I
). The results of Jarvis et al (1998)
showed that cytotoxicity (expressed as inhibition of cell proliferation) correlated with the total production of trichothecenes (both simple and macrocyclic). The three most toxic isolates in Jarvis et al (1998)
[JS58–02 (= IBT 9820), JS58–17 (= IBT 9821) and JS58–18 (= IBT 9819)] and one of medium toxicity [JS51–11 (= IBT 9808)] were all identified as S. chartarum and produced macrocyclic trichothecenes in our study, whereas the four less toxic isolates [JS58–07 (= IBT 9822), JS58–15 (= IBT 9810), JS51–05 (= IBT 9812) and JS63–01 (= IBT 9814)] were identified as atranone-producing S. chartarum. The last two isolates [JS51–08 (= IBT 98230) and JS58–06 (= IBT 9825)], showing low toxicity in Jarvis et al (1998)
were identified in this study as Stachybotrys sp. Group A and produced atranones. This suggests that the three Stachybotrys taxa/chemotypes have different inhibitory properties towards cell proliferation and agrees very well with our findings.
The same ten Stachybotrys isolates from Cleveland were also examined by Vesper et al (1999, 2000a)
(marked with in Table I ), in addition to two isolates from a culture collection [NC-1 (= ATCC 16026) and NC-4 (= ATCC 26303)]. They found that six [JS58–02 (= IBT 9820), JS58–17 (= IBT 9821), JS58–18 (= IBT 9819), JS51–11 (= IBT 9808), NC-1 (= IBT 9768) and NC-4 (= IBT 9769)] out of the above-mentioned 12 isolates were either high or intermediate in toxicity expressed as protein synthesis inhibition. In our study, all six were identified as macrocyclic trichothecene-producing S. chartarum. Isolates JS58–07 (= IBT 9822), JS58–15 (= IBT 9810), JS51–05 (= IBT 9812) and JS63–01 (= IBT 9814), identified as atranone-producing S. chartarum in our study, were found by Vesper et al (1999)
to have low toxicity. The two Stachybotrys sp. Group A isolates in our study, JS51–08 (= IBT 9823) and JS58–06 (= IBT 9825), were also low in toxicity according to Vesper et al (1999)
. Their results on toxicity are parallel to ours, but their results on production of a hemolysin, later identified as stachylysin (Vesper et al 2001
) do not correspond with either the toxicity or taxonomic groupings.
A set of 20 Finnish Stachybotrys isolates (HT isolates marked with 
in Table I
) was examined by Routsalainen et al (1998)
. They reported that seven Stachybotrys isolates (HT-401, HT-435, HT-502, HT-503, HT-513, HT-518 and HT-520) were able to induce TNF-
and IL-6 in macrophages, but did not induce ROS or cause cytotoxic effects on the macrophages. These seven were identified as atranone-producing S. chartarum isolates in our study. They also reported that isolate HT-016 was the only one that did not induce ROS, TNF- and IL-6 nor cause a cytotoxic effect in macrophages (Routsalainen et al 1998
). Results in our study show that HT-016 (= IBT 9714) belonged to Stachybotrys sp. Group A. The remaining 12 Stachybotrys isolates (HT-072, HT-165, HT-248, HT-296, HT-386, HT-387, HT-391, HT-471, HT-522, HT-523, HT-530, and HT-569) in the study of Routsalainen et al (1998)
were able to cause cytotoxic effects, but did not induce TNF- and IL-6 production in macrophages. All but one of these isolates [HT-523 (= IBT 9708)] belonged to the macrocyclic trichothecene-producing S. chartarum. This indicates that the three Stachybotrys taxa/chemotypes have different cytotoxic and inflammatory properties towards macrophages and corresponds very well with our findings.
The existence of three different taxa/chemotypes of Stachybotrys in water-damaged buildings can explain the variations or inconsistencies in toxicity and inflammation that have been reported in recent papers (Jarvis et al 1998
, Routsalainen et al 1998
, Vesper et al 1999
, Vesper et al 2001
). The growth characteristics and the metabolite profiles of isolates within the different taxa/chemotypes of Stachybotrys were the same whether they came from Cleveland, Ohio, Finland or Denmark. If it is assumed that this differentiation into three distinct Stachybotrys taxa/chemotypes is correct and that they all are present in the same water-damaged building, they should be addressed separately with respect to their toxic and inflammatory potentials. The taxon identified as Stachybotrys sp. Group A is a low inhibitor of protein synthesis and does not induce inflamation or toxicity towards macrophages. The atranone-producing chemotype of S. chartarum does not induce toxicity to macrophages, but instead induces inflamation and exhibits moderate inhibition of protein synthesis. The macrocyclic trichothecene-producing chemotype of S. chartarum, does not induce any inflammatory response in macrophages, but is highly toxic to macrophages and is a strong protein synthesis inhibitor. The different modes of action suggest that the three Stachybotrys taxa/chemotypes also have unique metabolite profiles containing different specific components. It is possible that the production of spirocyclic drimanes, common to all three taxa/chemotypes, cover up some unknown component in one of the taxa/chemotypes, that alone or in combination with known metabolites, is responsible for idiopathic pulmonary hemorrhage in infants.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Accepted for publication October 15, 2001.
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LITERATURE CITED |
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