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Growth rates of three representative xerophilic fungi (A); Xeromyces bisporus FRR 3443, Eurotium amstelodami FRR 2792, and isolate JH06THAJ (see Tables 1 and 2) in relation to chaotropic and kosmotropic activities of culture media: (I) NaCl (4.28 M, 0.775 aw), (II) NaCl (3.59 M, 0.812 aw), (III) sucrose (2.34 M, 0.831 aw), (IV) PEG 400 (1.25 M, 0.855 aw), (V) glycerol (4.90 M, 0.828 aw), (VI) fructose (3.51 M, 0.829 aw), (VII) fructose (3.94 M, 0.804 aw), (VIII) fructose (4.36 M, 0.791 aw), (IX) glycerol (6.66 M, 0.747 aw), (X) ammonium nitrate (4.30 M, 0.855 aw) and (XI) ammonium nitrate (5.15 M, 0.817 aw). Values are means of three replicates and bars represent standard errors. The data approximate to a Normal distribution (see dotted line), although it may be that the osmotic stress or other stress parameters associated with kosmotropic stressors ultimately limit hyphal growth. Diagrammatic illustrations (B–E) of the way in which chaotropic and kosmotropic activities impact on macromolecule and membrane structure in relation to an unstressed cell (B); in a chaotrope (e.g. urea)-stressed cell (C), a kosmotrope (e.g. sucrose)-stressed cell (D), and a cell exposed to both chaotropes and kosmotropes (E).
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Environments that are hostile to life are characterized by reduced microbial activity which results in poor soil- and plant-health, low biomass and biodiversity, and feeble ecosystem development. Whereas the functional biosphere may primarily be constrained by water activity (a(w)) the mechanism(s) by which this occurs have not been fully elucidate...
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... Driving freezing points to a range where liquid water could currently persist near the surface of Mars requires high enough concentrations of (per)chlorate salts to lower the a w below ∼0.6, the known limit of life (Grant, 2004;Schneegurt, 2012;Rummel et al., 2014;Primm et al., 2017;Pál and Kereszturi, 2020;Rivera-Valentín et al., 2020). Growth at record low a w previously has been demonstrated with fungi in high sugars and salts (Pitt and Christian, 1968;Williams and Hallsworth, 2009). ...
... Their resistant perennating structures give them additional survivability under conditions non-permissive for growth. Fungi currently hold the record for growth at the lowest a w (Pitt and Christian, 1968;Williams and Hallsworth, 2009). Therefore, discussions of planetary protection need to include salinotolerant fungi (Leo and Onofri, 2023). ...
Spacecraft can carry microbial contaminants from spacecraft assembly facilities (SAFs) to the cold arid surface of Mars that may confound life detection missions or disrupt native ecosystems. Dry hygroscopic sulphate and (per)chlorate salts on Mars may absorb atmospheric humidity and deliquesce at certain times to produce dense brines, potential sources of liquid water. Microbial growth is generally prohibited under the non-permissive condition of extremely low water activity in the frigid potential brines on Mars. Here we challenged the microbial community from samples of the Jet Propulsion Laboratory SAF with the extreme chemical conditions of brines relevant to Mars. Enrichment cultures in SP medium supplemented with 50% MgSO 4 or 20% NaClO 3 were inoculated from washes of SAF floor wipes. Samples were taken for each of the first four weeks and then at six months after inoculation to follow changes in the SAF microbial community under high salinity for long periods. Metagenomic DNA extracts of community samples were examined by Illumina sequencing of 18S rRNA gene sequences using fungal primers. The fungal assemblage during the first month of enrichment was predominantly common Ascomycetes, primarily Saccharomyete yeasts. Basidiomycetes were detected, mainly in the Microbotryomycetes and Tremellomycetes. Fungi were much less abundant in enrichment cultures at 50% MgSO 4 than at 20% NaClO 3 . After 6 months of enrichment, few fungi remained. Microbes persisting from the JPL SAF microbial community in aged cultures enriched at extreme salinities might be the most capable of subsequently surviving and proliferating at the near surface of Mars. The SAF fungal assemblage did not survive and proliferate as well as the SAF bacterial community.
... Certain cations like magnesium and calcium are chaotropic, meaning destabilizing, causing loss in cell function. The complex aspects of chaotropicity on life is an area of ongoing research and reviews can be found elsewhere [30,31]. Overall, the influence of chaotropic ions on microbial activity in salt cavern brine remains unexplored. ...
Hydrogen will be one of the key components for renewable energy storage in the future energy systems as it can be stored in significant volumes to overcome daily to seasonal energy fluctuations. Subsurface storage in salt caverns will be a first step. These caverns are created by solution mining in underground salt formations. Despite the high salinity in this environment, salt caverns harbor microbial life. These microorganisms can not only survive in these caverns by using unique adaptation mechanisms, but they actually cause several risks to hydrogen storage. Different metabolisms can use hydrogen as electron donor, leading to hydrogen loss and in the worst case also to H2S formation. The knowledge on salt cavern microbiology and subsequent possible effects of hydrogen is still in its infancy and only a limited number of salt caverns have been investigated so far. This review summarizes the current knowledge and key questions about halophilic (salt-loving) microbes, their adaptation strategies, their origin and potential consequences of their metabolisms. It also discusses the major factors influencing microbial activities and potential risks. This review emphasizes that more research and field trials with extensive microbial monitoring are needed before hydrogen storage in a biologically active system can be safely achieved at a global scale.
... For example, a w less than 0.91 and 0.7 is typically not conducive for bacterial replication or fungal growth, respectively (Manzoni et al., 2012;Lebre et al., 2017). However, many organisms are capable of living and growing below these levels (Williams and Hallsworth, 2009;Stevenson et al., 2015aStevenson et al., , 2015b. 6.3.4.2. ...
Scientific ideas about the potential existence of life elsewhere in the universe are predominantly informed by knowledge about life on Earth. Over the past ∼4 billion years, life on Earth has evolved into millions of unique species. Life now inhabits nearly every environmental niche on Earth that has been explored. Despite the wide variety of species and diverse biochemistry of modern life, many features, such as energy production mechanisms and nutrient requirements, are conserved across the Tree of Life. Such conserved features help define the operational parameters required by life and therefore help direct the exploration and evaluation of habitability in extraterrestrial environments. As new diversity in the Tree of Life continues to expand, so do the known limits of life on Earth and the range of environments considered habitable elsewhere. The metabolic processes used by organisms living on the edge of habitability provide insights into the types of environments that would be most suitable to hosting extraterrestrial life, crucial for planning and developing future astrobiology missions. This chapter will introduce readers to the breadth and limits of life on Earth and show how the study of life at the extremes can inform the broader field of astrobiology.
... For example, seawater has an a w of~0.98, most microbes cease cell division below 0.9, and fewer than 10 prokaryotic strains have been shown to continue cell division at a w < 0.755 (1)(2)(3)(4). The lowest a w reported to sustain prokaryotic cell division in pure culture is 0.635, and extrapolations from the pure culture observations suggest a lower limit of 0.611 (1). ...
Hypersaline brines provide excellent opportunities to study extreme microbial life. Here, we investigated anabolic activity in nearly 6000 individual cells from solar saltern sites with water activities ( a w ) ranging from 0.982 to 0.409 (seawater to extreme brine). Average anabolic activity decreased exponentially with a w , with nuanced trends evident at the single-cell level: The proportion of active cells remained high (>50%) even after NaCl saturation, and subsets of cells spiked in activity as a w decreased. Intracommunity heterogeneity in activity increased as seawater transitioned to brine, suggesting increased phenotypic heterogeneity with increased physiological stress. No microbial activity was detected in the 0.409- a w brine (an MgCl 2 -dominated site) despite the presence of cell-like structures. Extrapolating our data, we predict an a w limit for detectable anabolic activity of 0.540, which is beyond the currently accepted limit of life based on cell division. This work demonstrates the utility of single-cell, metabolism-based techniques for detecting active life and expands the potential habitable space on Earth and beyond.
... A. penicillioides is a xerophilic fungus commonly found in lowmoisture environments such as indoor air and house dust (41,42). Its presence has been suggested to contribute to the reproduction of D. pteronyssinus (43). ...
... Its presence has been suggested to contribute to the reproduction of D. pteronyssinus (43). Notably, both A. penicillioides and Penicillium cinerascens, found in D. pteronyssinus, possess antibacterial properties (34)(35)(36)(37)(38)(39)(40)(41)(42)(43)(44)(45)(46). Similar to our study, Saccharomyces cerevisiae, Aspergillus, and Candida were reported in D. pteronyssinus in other studies (30,32,47,48). ...
Understanding the house dust mites (HDMs) microbiome is crucial due to its potential effects on the development of allergic diseases. In 1998, our laboratory collected Dermatophagoides farinae and D. pteronyssinus from beds in a Korean household and began cultivating these HDMs. Our laboratory has been actively investigating several topics about HDMs in recent years, including the bacterial and fungal microbiome and their interactions, as well as the impact of the HDM microbiome on airway inflammation. To study the D. farinae microbiome, we employed high-throughput sequencing of the 16S rDNA amplicons. The results revealed that the two most abundant bacteria were Enterococcus faecalis and Bartonella spp. In contrast, we found almost no bacteria in D. pteronyssinus . By inoculating bacteria to HDMs, we found that D. farinae is more susceptible to bacteria than D. pteronyssinus. This susceptibility was associated with the presence of certain fungal species in D. pteronyssinus . Additionally, we have recently made efforts to produce HDMs with reduced levels of symbiotic bacteria. We believe that standardizing and controlling the microbiome in HDMs are crucial steps for the future development and improvement of allergic immunotherapies.
... A. atacamensis also exhibited high tolerance to sorbitol and glycerol, which considerably limit the water availability when present at high concentrations in media. A. atacamensis as well as Xeromyces bisporus (Pitt and Hocking, 2009;Williams and Hallsworth, 2009) had preference to grow in highly xerophilic media containing 2.5 and 5.13 M of sorbitol and glycerol, respectively (Figures 1-3). X. bisporus was described as the first fungus that showed extremely high tolerance to chaotropic conditions, being able to grow in the presence of 7.6 M of the chaotropic osmolyte glycerol (Williams and Hallsworth, 2009). ...
... A. atacamensis as well as Xeromyces bisporus (Pitt and Hocking, 2009;Williams and Hallsworth, 2009) had preference to grow in highly xerophilic media containing 2.5 and 5.13 M of sorbitol and glycerol, respectively (Figures 1-3). X. bisporus was described as the first fungus that showed extremely high tolerance to chaotropic conditions, being able to grow in the presence of 7.6 M of the chaotropic osmolyte glycerol (Williams and Hallsworth, 2009). However, unlike A. atacamensis, X. bisporus is intolerant to NaCl (Pitt and Hocking, 1977). ...
Obligate halophily is extremely rare in fungi. Nevertheless, Aspergillus atacamensis (strain EXF-6660), isolated from a salt water-exposed cave in the Coastal Range hills of the hyperarid Atacama Desert in Chile, is an obligate halophile, with a broad optimum range from 1.5 to 3.4 M of NaCl. When we tested its ability to grow at varied concentrations of both kosmotropic (NaCl, KCl, and sorbitol) and chaotropic (MgCl 2 , LiCl, CaCl 2 , and glycerol) solutes, stereoscopy and laser scanning microscopy revealed the formation of phialides and conidia. A. atacamensis EXF-6660 grew up to saturating levels of NaCl and at 2.0 M concentration of the chaotropic salt MgCl 2 . Our findings confirmed that A. atacamensis is an obligate halophile that can grow at substantially higher MgCl 2 concentrations than 1.26 M, previously considered as the maximum limit supporting prokaryotic life. To assess the fungus’ metabolic versatility, we used the phenotype microarray technology Biolog FF MicroPlates. In the presence of 2.0 M NaCl concentration, strain EXF-6660 metabolism was highly versatile. A vast repertoire of organic molecules (~95% of the substrates present in Biolog FF MicroPlates) was metabolized when supplied as sole carbon sources, including numerous polycyclic aromatic hydrocarbons, benzene derivatives, dyes, and several carbohydrates. Finally, the biotechnological potential of A. atacamensis for xenobiotic degradation and biosolid treatment was investigated. Interestingly, it could remove biphenyls, diphenyl ethers, different pharmaceuticals, phenols, and polyaromatic hydrocarbons. Our combined findings show that A. atacamensis EXF-6660 is a highly chaotolerant, kosmotolerant, and xerotolerant fungus, potentially useful for xenobiotic and biosolid treatments.
... targets within cells, interactions with different enzymes are reported due to their chaotropic and hydrophobic properties. For example, chaotropic compounds such as ethanol and MgCl 2 are able to inhibit β-galactosidase activity and the addition of protective agents (e.g., betaine) can reverse this inhibition depending on the stressor , a principle confirmed using agar gel-point assays (Alves et al., 2015) and whole-cell systems (Hallsworth et al., 2007;Stevenson et al., 2015;Stevenson, Hamill, Medina, et al., 2017;Williams & Hallsworth, 2009). Unlike chaotropic solutes, hydrophobic compounds do not seem to exert inhibitory activity on hydrophilic biomacromolecules due to their low solubility and limited interactions with hydrophilic domains . ...
Fungi and antifungal compounds are relevant to the United Nation's Sustainable Development Goals. However, the modes‐of‐action of antifungals—whether they are naturally occurring substances or anthropogenic fungicides—are often unknown or are misallocated in terms of their mechanistic category. Here, we consider the most effective approaches to identifying whether antifungal substances are cellular stressors, toxins/toxicants (that are target‐site‐specific), or have a hybrid mode‐of‐action as toxin–stressors (that induce cellular stress yet are target‐site‐specific). This newly described ‘toxin–stressor’ category includes some photosensitisers that target the cell membrane and, once activated by light or ultraviolet radiation, cause oxidative damage. We provide a glossary of terms and a diagrammatic representation of diverse types of stressors, toxic substances, and toxin–stressors, a classification that is pertinent to inhibitory substances not only for fungi but for all types of cellular life. A decision‐tree approach can also be used to help differentiate toxic substances from cellular stressors (Curr Opin Biotechnol 2015 33: 228–259). For compounds that target specific sites in the cell, we evaluate the relative merits of using metabolite analyses, chemical genetics, chemoproteomics, transcriptomics, and the target‐based drug‐discovery approach (based on that used in pharmaceutical research), focusing on both ascomycete models and the less‐studied basidiomycete fungi. Chemical genetic methods to elucidate modes‐of‐action currently have limited application for fungi where molecular tools are not yet available; we discuss ways to circumvent this bottleneck. We also discuss ecologically commonplace scenarios in which multiple substances act to limit the functionality of the fungal cell and a number of as‐yet‐unresolved questions about the modes‐of‐action of antifungal compounds pertaining to the Sustainable Development Goals.
... Incubations were carried out at temperatures from 2 to 50 • C. Eurotium halophilicum exhibited water-activity windows for germination and growth that spanned from ≥0.961 to 0.651, with a maximum rate of spore germination at around 0.900 water activity and no germination at 0.995 water activity [47]. The fungus could also germinate readily over the entire pH range tested, and had an optimum germination temperature of 30 • C, which is typical of other extremely xerophilic fungi [47,50]. We strongly suspect that E. halophilicum uses a multi-faceted strategy to attain these levels of stress tolerance (including production of microfilaments, compatible solutes, and extracellular polymeric substances, and the use of ion/salts to obtain vapour-phase water and regulate water activity in the form of brines). ...
... Indeed, if left unchecked, global warming may ultimately impair the habitability of Earth's surface [93]. The ecology of E. halophilicum is complex in as much as-like other fungal xerophiles-this species is commonly found on dry surfaces in nature and surfaces of artifacts and dust particles [50,65,[94][95][96]. Global climate change is causing various perturbations at the regional scale, at some places/times causing drought and at others causing floods. ...
Eurotium halophilicum is psychrotolerant, halophilic, and one of the most-extreme xerophiles in Earth’s biosphere. We already know that this ascomycete grows close to 0 °C, at high NaCl, and—under some conditions—down to 0.651 water-activity. However, there is a paucity of information about how it achieves this extreme stress tolerance given the dynamic water regimes of the surface habitats on which it commonly occurs. Here, against the backdrop of global climate change, we investigated the biophysical interactions of E. halophilicum with its extracellular environment using samples taken from the surfaces of library books. The specific aims were to examine its morphology and extracellular environment (using scanning electron microscopy for visualisation and energy-dispersive X-ray spectrometry to identify chemical elements) and investigate interactions with water, ions, and minerals (including analyses of temperature and relative humidity conditions and determinations of salt deliquescence and water activity of extracellular brine). We observed crystals identified as eugsterite (Na4Ca(SO4)3·2H2O) and mirabilite (Na2SO4·10H2O) embedded within extracellular polymeric substances and provide evidence that E. halophilicum uses salt deliquescence to maintain conditions consistent with its water-activity window for growth. In addition, it utilizes a covering of hair-like microfilaments that likely absorb water and maintain a layer of humid air adjacent to the hyphae. We believe that, along with compatible solutes used for osmotic adjustment, these adaptations allow the fungus to maintain hydration in both space and time. We discuss these findings in relation to the conservation of books and other artifacts within the built environment, spoilage of foods and feeds, the ecology of E. halophilicum in natural habitats, and the current episode of climate change.
... As a chaotropic ion, perchlorate is destabilizing biomacromolecules such as proteins (Salvi et al., 2005) or glycan (i.e. polysaccharide) macromolecules (Williams & Hallsworth, 2009). The fungal cell wall of D. hansenii's close relative, S. cerevisiae, consists of approximately 85% glycans (incl. ...
If life exists on Mars, it would face several challenges including the presence of perchlorates, which destabilize biomacromolecules by inducing chaotropic stress. However, little is known about perchlorate toxicity for microorganism on the cellular level. Here we present the first proteomic investigation on the perchlorate‐specific stress responses of the halotolerant yeast Debaryomyces hansenii and compare these to generally known salt stress adaptations. We found that the responses to NaCl and NaClO4‐induced stresses share many common metabolic features, e.g., signaling pathways, elevated energy metabolism, or osmolyte biosynthesis. Nevertheless, several new perchlorate‐specific stress responses could be identified, such as protein glycosylation and cell wall remodulations, presumably in order to stabilize protein structures and the cell envelope. These stress responses would also be relevant for life on Mars, which ‐ given the environmental conditions ‐ likely developed chaotropic defense strategies such as stabilized confirmations of biomacromolecules and the formation of cell clusters. This article is protected by copyright. All rights reserved.
... Moreover, the mitogen-activated protein kinase (MAPK) pathway, involved in germ tube elongation, branching, and hyphal fusion, is stimulated by conditions of low a w in many xerotolerant fungal species [44]. Notably, fungi can modulate their membrane and cell wall structure to counteract chaotropic and kosmotropic activity caused by solutes [45]; the chaophilic X. bisporus, for instance, maintains low membrane unsaturation indices [46]. ...
Extreme environments on Earth are typically devoid of macro life forms and are inhabited predominantly by highly adapted and specialized microorganisms. The discovery and persistence of these extremophiles provides tools to model how life arose on Earth and inform us on the limits of life. Fungi, in particular, are among the most extreme-tolerant organisms with highly versatile lifestyles and stunning ecological and morphological plasticity. Here, we overview the most notable examples of extremophilic and stress-tolerant fungi, highlighting their key roles in the functionality and balance of extreme ecosystems. The remarkable ability of fungi to tolerate and even thrive in the most extreme environments , which preclude most organisms, have reshaped current concepts regarding the limits of life on Earth.
