Health Effects of Wallemia

 

 
Zajc J, Gunde-Cimerman N. The Genus Wallemia-From Contamination of Food to Health Threat. Microorganisms. 2018 May 21;6(2). PMID: 29883408

The fungal genus Wallemia of the order Wallemiales (Wallemiomycotina, Basidiomycota) comprises the most xerotolerant, xerophilic and also halophilic species worldwide. Wallemia spp. are found in various osmotically challenged environments, such as dry, salted, or highly sugared foods, dry feed, hypersaline waters of solar salterns, salt crystals, indoor and outdoor air, and agriculture aerosols. To date, only strains of W. sebi, W. mellicola and W. muriae have been reported to be related to human health problems, as either allergological conditions (e.g., farmer’s lung disease) or rare subcutaneous/cutaneous infections. Therefore, this allergological and infective potential, together with the toxins that the majority of Wallemia spp. produce even under saline conditions, defines these fungi as filamentous food-borne pathogenic fungi.

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Health Research

Desroches TC, McMullin DR, Miller JD. Extrolites of Wallemia sebi, a very common fungus in the built environment. Indoor Air. 2014 Oct;24(5):533-42. PMID: 24471934

Wallemia sebi has been primarily known as a spoilage fungus of dried, salted fish and other foods that are salty or sweet. However, this fungus is also very common in house dust. IgE sensitization to W. sebi has been long reported from housing and occupational exposures. Strains from food have been reported to produce a number of compounds with modest toxicity. Strains from the built environment in Canada produced a number of metabolites including the known compound walleminone and a new compound 1-benzylhexahydroimidazo [1,5-α] pyridine-3,5-dione which we call wallimidione. Based on an in silico analysis, wallimidione is likely the most toxic of the metabolites reported to date from W. sebi. We found that the primary human antigen of W. sebi is a 47 kDa excreted cellulase present in high concentrations in W. sebi arthrospores. This species is a basidiomycete and, unsurprisingly, the antigen was not found in extracts of other fungi common in the built environment, all ascomycetes.

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Wood GM, Mann PJ, Lewis DF, Reid WJ, Moss MO. Studies on a toxic metabolite from the mould Wallemia. Food Addit Contam. 1990 Jan-Feb;7(1):69-77. PMID: 2106458

While monitoring the occurrence of toxigenic moulds in foods, using a bioassay screen, it was shown that an isolate of Wallemia sebi produced toxic effects in several of the bioassays. The minimum inhibitory dose of walleminol A in the bioassays is approximately 50 micrograms/ml, which is comparable with a number of mycotoxins such as citrinin and penicillic acid.

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Sakamoto T, Torii S, Yamada M, Urisu A, Iguchi H, Ueda M, Matsuda Y. Allergenic and antigenic activities of the osmophilic fungus Wallemia sebi asthmatic patients. Arerugi. 1989 Apr;38(4):352-9. PMID: 2783035

Recently large amounts of Wallemia sebi, a species of osmophilic fungi, have been detected in house dust by low water activity media. The allergenic activity of W. sebi was examined by skin prick tests and radioallergosorbent tests (RAST) in 74 asthmatic patients (mean age 11.7, range 6-32). In the skin prick tests, W. sebi extract, A. fumigatus extract and house dust extract elicited positive reactions in 4 (5.4%), 4 (5.4%) and 51 (68.9%) patients, respectively. RAST showed positive results in 14 subjects (18.9%) for W. sebi extract, in 8 (10.8%) for A. fumigatus extract and in 59 (79.7%) for house dust extract. These results indicated that some asthmatic individuals showed immediate type hypersensitivity to W. sebi, which means this fungal species may be important as a causative agent in atopic diseases.

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Sakamoto T, Urisu A, Yamada M, Matsuda Y, Tanaka K, Torii S. Studies on the osmophilic fungus Wallemia sebi as an allergen evaluated by skin prick test and radioallergosorbent test. Int Arch Allergy Appl Immunol. 1989;90(4):368-72. PMID: 2613343

Recently, Wallemia sebi, a species of osmophilic fungi, has been abundantly detected in house dust using low water activity media. In this study, allergenic activity of W. sebi was assessed by skin prick test and radioallergosorbent test (RAST) in 74 asthmatic patients ranging from 6 to 32 years of age. Aspergillus fumigatus and house dust were used for comparison. In skin prick test, W. sebi extract, A. fumigatus extract and house dust extract elicited positive reactions in 4 (5.4%), 4 (5.4%) and 51 (68.9%) patients, respectively. RAST showed positive results in 14 subjects (18.9%) for W. sebi extract, in 8 (10.8%) for A. fumigatus extract and in 59 (79.7%) for house dust extract. These results indicated that some asthmatic individuals showed immediate-type hypersensitivity to W. sebi, and which means this fungal species may be of importance to atopic diseases as a causative agent.

 

Growth Research

Gunde-Cimerman N, Plemenitaš A, Oren A. Strategies of adaptation of microorganisms of the three domains of life to high salt concentrations. FEMS Microbiol Rev. 2018 May 1;42(3):353-375. PMID: 29529204

Hypersaline environments with salt concentrations up to NaCl saturation are inhabited by a great diversity of microorganisms belonging to the three domains of life. They all must cope with the low water activity of their environment, but different strategies exist to provide osmotic balance of the cells’ cytoplasm with the salinity of the medium. Here, we review the mechanisms of osmotic adaptation in a number of model organisms, including the the basidiomycetous Wallemia ichthyophaga, which use glycerol and other compatible solutes.

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Gostinčar C, Gunde-Cimerman N. Overview of Oxidative Stress Response Genes in Selected Halophilic Fungi. Genes (Basel). 2018 Mar 6;9(3). PMID: 29509668

Exposure of microorganisms to stress, including to high concentrations of salt, can lead to increased production of reactive oxygen species in the cell. According to our results, Wallemia ichthyophaga can survive salinities detrimental to most other organisms with only a moderate number of oxidative stress response genes.

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Nguyen HD, Jančič S, Meijer M, Tanney JB, Zalar P, Gunde-Cimerman N, Seifert KA. Application of the phylogenetic species concept to Wallemia sebi from house dust and indoor air revealed by multi-locus genealogical concordance. PLoS One. 2015 Mar 23;10(3):e0120894. PMID: 25799362

A worldwide survey of Wallemia occurring in house dust and indoor air was conducted. The isolated strains were identified as W. sebi and W. muriae. Geographically, W. muriae was only found in Europe, W. sebi clade 3 was only found in Canada, W. sebi clade 4 was found in subtropical regions, while W. sebi clade 1 and 2 were found worldwide. Haplotype analysis showed that W. sebi clades 1 and 2 had multiple haplotypes while W. sebi clades 3 and 4 had one haplotype and may have been under sampled. We describe W. sebi clades 2, 3, and 4 as new species in a companion study.

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Zajc J, Džeroski S, Kocev D, Oren A, Sonjak S, Tkavc R, Gunde-Cimerman N. Chaophilic or chaotolerant fungi: a new category of extremophiles? Front Microbiol. 2014 Dec 23;5:708. PMID: 25566222

It is well known that few halophilic bacteria and archaea as well as certain fungi can grow at the highest concentrations of NaCl. Fungi from diverse (extreme) environments were tested for their ability to grow at the highest concentrations of kosmotropic and chaotropic salts ever recorded to support life. The majority of fungi showed preference for relatively high concentrations of kosmotropes. However, our study revealed the outstanding tolerance of several fungi to high concentrations of MgCl2 (up to 2.1 M) or CaCl2 (up to 2.0 M) without compensating kosmotropic salts. Few species, for instance Hortaea werneckii, Eurotium amstelodami, Eurotium chevalieri and Wallemia ichthyophaga, are able to thrive in media with the highest salinities of all salts (except for CaCl2 in the case of W. ichthyophaga).

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Deschuyffeleer N, Vermeulen A, Daelman J, Castelein E, Eeckhout M, Devlieghere F. Modelling of the growth/no growth interface of Wallemia sebi and Eurotium herbariorum as a function of pH, aw and ethanol concentration. Int J Food Microbiol. 2015 Jan 2;192:77-85. PMID: 25317503

High sugar products (sugar content > 50%) are generally considered to be stable against all forms of microbial spoilage during a prolonged shelf life of several months. However, one specific subgroup of micro-organisms, the xerophilic moulds, can develop quite fast on the surface of food products with a reduced water activity (< 0.85). The chance whether these xerophilic moulds are able to grow on the food product depends on the combination of intrinsic factors (e.g., water activity and pH) and the storage conditions (e.g., temperature). This study examines the development of growth/no growth models for the xerophilic moulds Wallemia sebi and Eurotium herbariorum in a sugar rich broth. In this research, a water activity between 0.75 and 0.90, a pH between 5.0 and 6.2, an ethanol concentration between 0% and 5% (g EtOH/g H2O) and their interactions were tested. The obtained models were also validated in a chocolate-based food product (ganache). The resulting growth/no growth models show that the growth of W. sebi and E. herbariorum can be inhibited for a prolonged time (> 3 months) if an ethanol concentration of 5% on the water phase is present in the food product, irrespective of water activity values between 0.89 and 0.755.

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Plemenitaš A, Lenassi M, Konte T, Kejžar A, Zajc J, Gostinčar C, Gunde-Cimerman N. Adaptation to high salt concentrations in halotolerant/halophilic fungi: a molecular perspective. Front Microbiol. 2014 May 5;5:199. PMID: 24860557

Discovery of the extremely halotolerant and adaptable fungus Hortaea werneckii and the obligate halophile Wallemia ichthyophaga introduced two new model organisms into studies on the mechanisms of salt tolerance in eukaryotes. W. ichthyophaga requires at least 1.5 M NaCl for growth, but also grows in up to 5 M NaCl. Our studies have revealed the novel and intricate molecular mechanisms used by these fungi to combat high salt concentrations, which differ in many aspects between the extremely halotolerant H. werneckii and the halophilic W. ichthyophaga.

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Zajc J, Kogej T, Galinski EA, Ramos J, Gunde-Cimerman N. Osmoadaptation strategy of the most halophilic fungus, Wallemia ichthyophaga, growing optimally at salinities above 15% NaCl. Appl Environ Microbiol. 2014 Jan;80(1):247-56. PMID: 24162565

Wallemia ichthyophaga is a fungus from the ancient basidiomycetous genus Wallemia (Wallemiales, Wallemiomycetes) that grows only at salinities between 10% (wt/vol) NaCl and saturated NaCl solution. Our results showed that growth on solid growth media was extremely slow and resulted in small colonies. On the other hand, in the liquid batch cultures, the specific growth rates of W. ichthyophaga were higher, and the biomass production increased with increasing salinities. The optimum salinity range for growth of W. ichthyophaga was between 15 and 20% (wt/vol) NaCl.

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Kralj Kunčič M, Zajc J, Drobne D, Pipan Tkalec Z, Gunde-Cimerman N. Morphological responses to high sugar concentrations differ from adaptation to high salt concentrations in the xerophilic fungi Wallemia spp. Fungal Biol. 2013 Jul-Aug;117(7-8):466-78. PMID: 23931114 

Fungi from the food-borne basidiomycetous genus Wallemia, which comprises Wallemia ichthyophaga, Wallemia muriae and Wallemia sebi, are among the most xerophilic organisms described. Wallemia ichthyophaga grew slowly in all of the sugar-based media, while W. muriae and W. sebi demonstrated better growth. Wallemia ichthyophaga adapted to the high glucose and honey concentrations with formation of larger cellular aggregates, while cell-wall thickness was increased only at the high glucose concentration. Adaptive responses show that the phylogenetically more distant W. ichthyophaga is better adapted to high salt conditions, whereas W. muriae and W. sebi cope better with a high sugar environment.

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Nguyen HD, Nickerson NL, Seifert KA. Basidioascus and Geminibasidium: a new lineage of heat-resistant and xerotolerant basidiomycetes. Mycologia. 2013 Sep-Oct;105(5):1231-50. PMID: 23709525

Hypersaline environments with salt concentrations up to NaCl saturation are inhabited by a great diversity of microorganisms belonging to the three domains of life. They all must cope with the low water activity of their environment, but different strategies exist to provide osmotic balance of the cells’ cytoplasm with the salinity of the medium. One option used by many halophilic Archaea and a few representatives of the Bacteria is to accumulate salts, mainly KCl and to adapt the entire intracellular machinery to function in the presence of molar concentrations of salts. A more widespread option is the synthesis or accumulation of organic osmotic, so-called compatible solutes. Here, we review the mechanisms of osmotic adaptation in a number of model organisms, including the KCl accumulating Halobacterium salinarum (Archaea) and Salinibacter ruber (Bacteria), Halomonas elongata as a representative of the Bacteria that synthesize organic osmotic solutes, eukaryotic microorganisms including the unicellular green alga Dunaliella salina and the black yeasts Hortaea werneckii and the basidiomycetous Wallemia ichthyophaga, which use glycerol and other compatible solutes. The strategies used by these model organisms and by additional halophilic microorganisms presented are then compared to obtain an integrative picture of the adaptations to life at high salt concentrations in the microbial world.

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Botić T, Kunčič MK, Sepčić K, Knez Z, Gunde-Cimerman N. Salt induces biosynthesis of hemolytically active compounds in the xerotolerant food-borne fungus Wallemia sebi. FEMS Microbiol Lett. 2012 Jan;326(1):40-6. PMID: 22092533

Wallemia sebi is a xerotolerant, ubiquitous, food-borne, mycotoxigenic fungus. An ethanol extract of its mycelium demonstrated a strong hemolytic activity, which was further enhanced at high salt concentrations in the growth medium. The W. sebi lytic activity on mammalian erythrocytes shows its potential involvement in the formation of lesions in subcutaneous infections, in farmer’s lung disease, and in consumption of food and feed that are contaminated with food-borne W. sebi.

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