Aureobasidium subglaciale

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Aureobasidium subglaciale
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Dothideomycetes
Order: Dothideales
Family: Dothioraceae
Genus: Aureobasidium
Species:
A. subglaciale
Binomial name
Aureobasidium subglaciale
Zalar, Gostincar, Gunde-Cimerman (2014)

Previously classified under the species complex Aureobasidium pullulans, Aureobasidium subglaciale is a black yeast-like, extremophile, ascomycete fungus that is found in extreme cold habitats. The species was originally isolated from subglacial ice of arctic glaciers. [1] [2] The first isolate of this species was obtained from subglacial ice of the Norwegian island Spitsbergen, one of the coldest places inhabited by humans. of Genomic data collected from specimens in the Aureobasidium pullulans complex justified distinction of four different species [1] [2]

Contents

Aureobasidium subglaciale is specifically known for its capability to grow and reproduce at low temperatures. The species could potentially be economically valuable, as recent research has shown promise for the use of A. subglaciale as a biocontrol agent for various post-harvest rot pathogens. The survival of the species at low temperatures is favorable for refrigerated conditions, making this particular species of Aureobasidium of prominent interest. [3] Due to the somewhat recent distinction of A. subglaciale from the A. pullulans species complex, much of the current research does not make the distinction between A. pullulans strains, and thus there is limited information on this species.

Taxonomy

Aureobasidium subglaciale is a member of the Ascomycota division of the kingdom Fungi. It belongs to the class Dothideomycetes, the largest and most diverse class in Ascomycota. The species falls under the order Dothideales and family Dothioraceae. The name subglaciale refers to the fungus being primarily found in subglacial ice. [1] The Aureobasidium genus was first classified in 1891 in Revue Générale de Botanique by Viala, P. and Boyer, G. The genomic differences observed between the four varieties of the A. pullulans species complex are larger than S. cerevisiae and three of its closest relatives. Phylogenetic analyses place the genus Aureobasidium closely related to Kabatiella, a genus known for causing eyespot on leaves. [1]

Morphology

When viewed under a microscope, A. subglaciale has been observed to have hyaline, smooth, thin-walled hyphae that are 2-10 μm wide. The hyphae are sometimes developed in conidiophore-like clusters. [1] Hyaline to dark brown conidia are produced from small denticles in dense groups. Conidia are extremely variable in size, and often have an indistinct hilum. [1] Conidia budding can be seen abundantly. [1] In culture, A. subglaciale is able to 10% NaCl concentrations in culture and grows well between 4°C and 25°C. Colonies on MEA/PDA media at 25°C attained 20 mm diameter after seven days and exhibited abundant sporulation. [1]

Ecology

So far, A. subglaciale specimens have only been isolated from a small number of cold environments, including refrigeration, as well as in radiation polluted soils. [3] [4] A. subglaciale strains are primarily found in subglacial ice or in moss during colder parts of the year.The species tolerates high salinity, radiation contamination, high heavy metal concentrations, and high UV radiation. Most of studied isolates, including the first discovered, were sourced from glaciers of the Norwegian island Spitsbergen. Little is known of the nutritional strategies of A. subglaciale, however genomic analyses show evidence of high metabolic versatility, with high concentrations proteins associated with plant and fungal cell wall degradation. [3]

Heavy metal and radiation tolerance allows A. subglaciale to colonize habitats typically thought to be unwelcoming for life. A strain of A. subglaciale was collected from radiation and heavy-metal polluted soil in the Xinjiang province in China. [4] The radioactive resistance of the strain was found to be associated with the presence of the stress-protecting disaccharide trehalose. Trehalose is primarily produced through the OtsA-OtsB pathway, [4] found in all prokaryotes and eukaryotes. Two highly involved enzymes in this process are trehalose-6-phosphate synthase (TPS) and vacuolar acidic trehalase (ATH), the prior accelerates trehalose production while the latter inhibits it. [4] Mutant strains can be created to overproduce TPS and underproduce ATH, leading to enhanced trehalose production. Mutant strains that overproduced trehalose displayed significantly enhanced resistance characteristics, especially to radiation. [4]

Stress-test experiments have shown that increased salinity triggers intracellular glycerol accumulation in A. subglaciale cultures. [5] Intracellular glycerol accumulation is known to be one of the primary fungal adaptations to salinity and cold stress. Glycerol helps to maintain intracellular osmotic pressure and prevents plasmolysis in high salinity environments; thus, the accumulation of this compound is common in salinity-adapted fungi. [6] Much of what contributes to halotolerance in fungi is still poorly understood, as there are many cell processes that are put under extreme stress under hypersaline conditions, and little is known about how this stress is managed. [7]

Human Significance

There have been several studies conducted that show potential for commercial uses of A. subglaciale as a biocontrol agent and as a bifunctional biocatalyst. At low temperatures, A. subglaciale efficiently transforms acetophenone to phenol via Baeyer-Villiger oxidation. Increasing reaction temperatures allow for changing the chemoselectivity of A. subglaciale F134, and this strain accepts several different aldehydes and ketones as substrates for these reactions. [8] Such microbial processes provide sustainable and energy-effective alternatives to the common ways in which chemicals are synthesized for commercial and medical use. Research has been conducted on the potential for the use of A. subglaciale as a biocontrol agent for post-harvest rot of fruits and vegetables. The ability of A. subglaciale to grow in refrigerated climates makes the species particularly appealing for this use. A. subglaciale strains out-performed other Aureobasidium strains in reducing Botrytis cinerea (grey mold) growth on tomatoes. [9] Another of the studied strains, Aureobasidium melanogeneum, was the least effective at limiting B. cinerea growth. This strain is also a human pathogen, so it is not acceptable for use as a biocontrol agent. A. pullulans produces very similar secondary metabolites and volatile organic compounds. [9] Moreover, A. pullulans has comparable efficacy against B. cinerea as A. subglaciale, however it does not grow nearly as well in refrigerated conditions. [9]

An important concern with regard for the biocontrol potential for A. subglaciale is how it attains iron, an essential growth and development compound, oxygen carrier, and enzyme cofactor. [3] A. subglaciale is able to access bioavailable iron in the environment through the production of siderophores. Siderophores are compounds with high affinity to bind iron. Strains of fungi that produce abundant siderophores have high potential for outcompeting plant pathogens, as iron is a severely limiting resource. All studied A. subglaciale strains in Zajc et al. 2022 produced siderophores, but produced different amounts and different types including the yellow hydroxamate, and the pink catechol siderophores. [3] The only other known producer of catecholate siderophores is Penicillium bilaii. [3] This finding warrants additional study into the properties of these compounds and their chemical importance to the fungus. [3] A. subglaciale visibly performed exceptionally against fungal pathogens B. cinerea and P. expansum on apples, further showing promise for the use of the species as a rot-prevention measure on various crops. On average A. subglaciale reduced necrosis on apples from C. acutatum and B. Cinerea by 74.4% and 71.6% respectively at 10 °C. [3] Aureobasidium pullulans is known to produce several important biotechnological compounds, such as the linear glucosic polysaccharide Pullulan, which has been used for food additive as well as environmental remediation agents. [10] Since A. subglaciale is so closely related to A. pullulans, it is likely to produce similar compounds. However, isolates of A. subglaciale are rare, and little research has been done on the various compounds produced by the strain that could be of economic use.

Little research has evaluated the potential of A. subglaciale as a human pathogen, but there is little evidence to support that potential. The previous grouping of A. subglaciale within the A. pullulans species complex raises concerns as to how much of the current research is valid for A. subglaciale specifically. Since cultures of A. subglaciale are rare and the fungus is extremely difficult to obtain from the environment, knowledge of this species is growing slowly.


See also

Related Research Articles

A halophile is an extremophile that thrives in high salt concentrations. In chemical terms, halophile refers to a Lewis acidic species that has some ability to extract halides from other chemical species.

Halotolerance is the adaptation of living organisms to conditions of high salinity. Halotolerant species tend to live in areas such as hypersaline lakes, coastal dunes, saline deserts, salt marshes, and inland salt seas and springs. Halophiles are organisms that live in highly saline environments, and require the salinity to survive, while halotolerant organisms can grow under saline conditions, but do not require elevated concentrations of salt for growth. Halophytes are salt-tolerant higher plants. Halotolerant microorganisms are of considerable biotechnological interest.

<i>Botrytis cinerea</i> Species of fungus

Botrytis cinerea is a necrotrophic fungus that affects many plant species, although its most notable hosts may be wine grapes. In viticulture, it is commonly known as "botrytis bunch rot"; in horticulture, it is usually called "grey mould" or "gray mold".

<i>Pseudomonas fluorescens</i> Species of bacterium

Pseudomonas fluorescens is a common Gram-negative, rod-shaped bacterium. It belongs to the Pseudomonas genus; 16S rRNA analysis as well as phylogenomic analysis has placed P. fluorescens in the P. fluorescens group within the genus, to which it lends its name.

<span class="mw-page-title-main">Allyl alcohol</span> Organic compound (CH2=CHCH2OH)

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<i>Rhodotorula</i> Genus of fungi

Rhodotorula is a genus of fungi in the class Microbotryomycetes. Most species are known in their yeast states which produce orange to red colonies when grown on Sabouraud's dextrose agar (SDA). The colour is the result of pigments that the yeast creates to block out certain wavelengths of light (620–750 nm) that would otherwise be damaging to the cell. Hyphal states, formerly placed in the genus Rhodosporidium, give rise to teliospores from which laterally septate basidia emerge, producing sessile basidiospores. Species occur worldwide and can be isolated from air, water, soil, and other substrates.

<i>Stenotrophomonas</i> Genus of bacteria

Stenotrophomonas is a genus of Gram-negative bacteria, comprising at least ten species. The main reservoirs of Stenotrophomonas are soil and plants. Stenotrophomonas species range from common soil organisms to opportunistic human pathogens ; the molecular taxonomy of the genus is still somewhat unclear.

<i>Eremothecium gossypii</i> Species of fungus

Eremothecium gossypii (also known as Ashbya gossypii) is a filamentous fungus or mold closely related to yeast, but growing exclusively in a filamentous way. It was originally isolated from cotton as a pathogen causing stigmatomycosis by Ashby and Nowell in 1926. This disease affects the development of hair cells in cotton bolls and can be transmitted to citrus fruits, which thereupon dry out and collapse (dry rot disease). In the first part of the 20th century, E. gossypii and two other fungi causing stigmatomycosis (Eremothecium coryli, Aureobasidium pullulans) made it virtually impossible to grow cotton in certain regions of the subtropics, causing severe economical losses. Control of the spore-transmitting insects - cotton stainer (Dysdercus suturellus) and Antestiopsis (antestia bugs) - permitted full eradication of infections. E. gossypii was recognized as a natural overproducer of riboflavin (vitamin B2), which protects its spores against ultraviolet light. This made it an interesting organism for industries, where genetically modified strains are still used to produce this vitamin.

<i>Aureobasidium pullulans</i> Species of fungus

Aureobasidium pullulans is a ubiquitous and generalistic black, yeast-like fungus that can be found in different environments. It is well known as a naturally occurring epiphyte or endophyte of a wide range of plant species without causing any symptoms of disease. A. pullulans has a high importance in biotechnology for the production of different enzymes, siderophores and pullulan. Furthermore, A. pullulans is used in biological control of plant diseases, especially storage diseases.

Pathogenic fungi are fungi that cause disease in humans or other organisms. Although fungi are eukaryotic, many pathogenic fungi are microorganisms. Approximately 300 fungi are known to be pathogenic to humans; their study is called "medical mycology". Fungal infections kill more people than either tuberculosis or malaria—about 2 million people per year.

<i>Hortaea werneckii</i> Species of fungus

Hortaea werneckii is a species of yeast in the family Teratosphaeriaceae. It is a black yeast that is investigated for its remarkable halotolerance. While the addition of salt to the medium is not required for its cultivation, H. werneckii can grow in close to saturated NaCl solutions. To emphasize this unusually wide adaptability, and to distinguish H. werneckii from other halotolerant fungi, which have lower maximum salinity limits, some authors describe H. werneckii as "extremely halotolerant".

<span class="mw-page-title-main">Wallemiomycetes</span> Class of fungi

The Wallemiomycetes are a class of fungi in the division Basidiomycota. It consists of the single order Wallemiales, containing the single family Wallemiaceae, which in turn contains the single genus Wallemia. The phylogenetic origin of the lineage was placed to various parts of Basidiomycota, but according to the analysis of a larger dataset it is a sister group of Agaricomycotina. The genus contains species of xerophilic molds that are found worldwide. The seven described species are distinguished by conidial size, xerotolerance, halotolerance, chaotolerance, growth temperature regimes, extracellular enzyme activity profiles, and secondary metabolite patterns. They are typically isolated from low-moisture foods, indoor air dust, salterns and soil. W. sebi is thought to be one of the causes of the hypersensitivity pneumonitis known as the farmer's lung disease, but since the other species were recognised and separated from W. sebi only recently, their role in the disease cannot be excluded.

Mycosporine-like amino acids (MAAs) are small secondary metabolites produced by organisms that live in environments with high volumes of sunlight, usually marine environments. The exact number of compounds within this class of natural products is yet to be determined, since they have only relatively recently been discovered and novel molecular species are constantly being discovered; however, to date their number is around 30. They are commonly described as “microbial sunscreens” although their function is believed not to be limited to sun protection. MAAs represent high potential in cosmetics, and biotechnological applications. Indeed, their UV-absorbing properties would allow to create products derived from natural photoprotectors, potentially harmless to the environment and efficient against UV damage.

Black yeasts, sometimes also black fungi, dematiaceous fungi, microcolonial fungi or meristematic fungi is a diverse group of slow-growing microfungi which reproduce mostly asexually. Only few genera reproduce by budding cells, while in others hyphal or meristematic (isodiametric) reproduction is preponderant. Black yeasts share some distinctive characteristics, in particular a dark colouration (melanisation) of their cell wall. Morphological plasticity, incrustation of the cell wall with melanins and presence of other protective substances like carotenoids and mycosporines represent passive physiological adaptations which enable black fungi to be highly resistant against environmental stresses. The term "polyextremotolerance" has been introduced to describe this phenotype, an example of which is the species Aureobasidium pullulans. Presence of 1,8-dihydroxynaphthalene melanin in the cell wall confers to the microfungi their characteristic olivaceous to dark brown/black colour.

<i>Wallemia ichthyophaga</i> Species of fungus

Wallemia ichthyophaga is one of the three species of fungi in the genus Wallemia, which in turn is the only genus of the class Wallemiomycetes. The phylogenetic origin of the lineage was placed to various parts of Basidiomycota, but according to the analysis of larger datasets it is a (495-million-years-old) sister group of Agaricomycotina. Although initially believed to be asexual, population genomics found evidence of recombination between strains and a mating type locus was identified in all sequenced genomes of the species.

Aureobasidium melanogenum, formerly known as Aureobasidium pullulans var. melanogenum is a ubiquitous black, yeast-like fungus that is found mainly in freshwater habitats. The species also includes strains causing human infections, which were previously classified as A. pullulans. It was named due to abundant melanin production and accumulation in the cell walls, which leads to dark green, brown or black appearance of the cells and colonies The species was established when the genomes of the four former varieties of Aureobasidium pullulans were sequenced and the large differences between them were discovered.

Aureobasidium namibiae, formerly known as Aureobasidium pullulans var. namibiae is a ubiquitous black, yeast-like fungus. It was described on the basis of only one strain isolated from dolomitic marble in Namibia. The species was established when the genomes of the four former varieties of Aureobasidium pullulans were sequenced and the large differences between them were discovered.

Wallemia mellicola is a xerophilic fungus of the phylum Basidiomycota, described in 2015 upon taxonomic revision of the species Wallemia sebi. A large amount of published research referring to W. sebi was likely actually performed on W. mellicola. An example of this is the sequencing of the W. mellicola genome, which was published under the name of W. sebi.

Fungal genomes are among the smallest genomes of eukaryotes. The sizes of fungal genomes range from less than 10 Mbp to hundreds of Mbp. The average genome size is approximately 37 Mbp in Ascomycota, 47 Mbp in Basidiomycota and 75 Mbp in Oomycota. The sizes and gene numbers of the smallest genomes of free-living fungi such as those of Wallemia ichthyophaga, Wallemia mellicola or Malassezia restricta are comparable to bacterial genomes. The genome of the extensively researched yeast Saccharomyces cerevisiae contains approximately 12 Mbp and was the first completely sequenced eukaryotic genome. Due to their compact size fungal genomes can be sequenced with less resources than most other eukaryotic genomes and are thus important models for research. Some fungi exist as stable haploid, diploid, or polyploid cells, others change ploidy in response to environmental conditions and aneuploidy is also observed in novel environments or during periods of stress.

References

  1. 1 2 3 4 5 6 7 8 Zalar, P.; Gostinčar, C.; de Hoog, G.S.; Uršič, V.; Sudhadham, M.; Gunde-Cimerman, N. (2008). "Redefinition of Aureobasidium pullulans and its varieties". Studies in Mycology. 61: 21–38. doi:10.3114/sim.2008.61.02. ISSN   0166-0616. PMC   2610310 . PMID   19287524.
  2. 1 2 Gostinčar, Cene; Ohm, Robin A; Kogej, Tina; Sonjak, Silva; Turk, Martina; Zajc, Janja; Zalar, Polona; Grube, Martin; Sun, Hui; Han, James; Sharma, Aditi; Chiniquy, Jennifer; Ngan, Chew Yee; Lipzen, Anna; Barry, Kerrie; Grigoriev, Igor V; Gunde-Cimerman, Nina (2014-07-01). "Genome sequencing of four Aureobasidium pullulans varieties: biotechnological potential, stress tolerance, and description of new species". BMC Genomics. 15: 549. doi: 10.1186/1471-2164-15-549 . ISSN   1471-2164. PMC   4227064 . PMID   24984952.
  3. 1 2 3 4 5 6 7 8 Zajc, Janja; Černoša, Anja; Sun, Xiaohuan; Fang, Chao; Gunde-Cimerman, Nina; Song, Zewei; Gostinčar, Cene (2022-07-26). "From Glaciers to Refrigerators: the Population Genomics and Biocontrol Potential of the Black Yeast Aureobasidium subglaciale". Microbiology Spectrum. 10 (4): –01455–22. doi: 10.1128/spectrum.01455-22 . PMC   9430960 .
  4. 1 2 3 4 5 Liu, Tingting; Zhu, Liying; Zhang, Zhiping; Huang, He; Zhang, Zhidong; Jiang, Ling (2017-12-14). "Protective role of trehalose during radiation and heavy metal stress in Aureobasidium subglaciale F134". Scientific Reports. 7 (1): 17586. doi: 10.1038/s41598-017-15489-0 . ISSN   2045-2322. PMC   5730648 .
  5. ↑ Turk, Martina; Gostinčar, Cene (2018-01-01). "Glycerol metabolism genes in Aureobasidium pullulans and Aureobasidium subglaciale". Fungal Biology. 122 (1): 63–73. doi:10.1016/j.funbio.2017.10.005. ISSN   1878-6146 . Retrieved 2023-11-04.
  6. ↑ Hohmann, Stefan (2002). "Osmotic Stress Signaling and Osmoadaptation in Yeasts". Microbiology and Molecular Biology Reviews. 66 (2): 300–372. doi:10.1128/mmbr.66.2.300-372.2002. PMC   120784 . PMID   12040128.
  7. ↑ Gostinčar, Cene; Lenassi, Metka; Gunde-Cimerman, Nina; Plemenitaš, Ana (2011-01-01). "Chapter 3 - Fungal Adaptation to Extremely High Salt Concentrations". In Allen I. Laskin, Sima Sariaslani, Geoffrey M. Gadd (ed.). Advances in Applied Microbiology. Vol. 77. Academic Press. pp. 71–96. Retrieved 2023-11-05.{{cite book}}: CS1 maint: multiple names: editors list (link)
  8. ↑ Shen, Liqun; Cang, Ran; Yang, Guang; Zeng, Anqi; Huang, He; Zhang, Zhigang (2020-12-01). "Aureobasidium subglaciale F134 is a bifunctional whole-cell biocatalyst for Baeyer–Villiger oxidation or selective carbonyl reduction controllable by temperature". Chinese Journal of Chemical Engineering. 28 (12): 3044–3051. doi:10.1016/j.cjche.2020.06.041. ISSN   1004-9541 . Retrieved 2023-11-05.
  9. 1 2 3 Di Francesco, Alessandra; Di Foggia, Michele; Zajc, Janja; Gunde-Cimerman, Nina; Baraldi, Elena (2020). "Study of the efficacy of Aureobasidium strains belonging to three different species: A. pullulans, A. subglaciale and A. melanogenum against Botrytis cinerea of tomato". Annals of Applied Biology. 177 (2): 266–275. doi:10.1111/aab.12627. ISSN   1744-7348 . Retrieved 2023-11-05.
  10. ↑ Cheng, Kuan-Chen; Demirci, Ali; Catchmark, Jeffrey M. (2011-10-01). "Pullulan: biosynthesis, production, and applications". Applied Microbiology and Biotechnology. 92 (1): 29–44. doi:10.1007/s00253-011-3477-y. ISSN   1432-0614 . Retrieved 2023-11-05.
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