Biophysical Manipulation of the Extracellular Environment by <i>Eurotium halophilicum</i>

<i>Eurotium halophilicum</i> 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 informa...

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Main Authors: Anna Micheluz, Flavia Pinzari, Edgard G. Rivera-Valentín, Sabrina Manente, John E. Hallsworth
Format: Article
Language:English
Published: MDPI AG 2022-12-01
Series:Pathogens
Subjects:
Online Access:https://www.mdpi.com/2076-0817/11/12/1462
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author Anna Micheluz
Flavia Pinzari
Edgard G. Rivera-Valentín
Sabrina Manente
John E. Hallsworth
author_facet Anna Micheluz
Flavia Pinzari
Edgard G. Rivera-Valentín
Sabrina Manente
John E. Hallsworth
author_sort Anna Micheluz
collection DOAJ
description <i>Eurotium halophilicum</i> 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 <i>E. halophilicum</i> 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 (Na<sub>4</sub>Ca(SO<sub>4</sub>)<sub>3</sub>·2H<sub>2</sub>O) and mirabilite (Na<sub>2</sub>SO<sub>4</sub>·10H<sub>2</sub>O) embedded within extracellular polymeric substances and provide evidence that <i>E. halophilicum</i> 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 <i>E. halophilicum</i> in natural habitats, and the current episode of climate change.
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spelling doaj.art-352b9c99f5f947518916154d23efa95e2023-11-24T17:13:07ZengMDPI AGPathogens2076-08172022-12-011112146210.3390/pathogens11121462Biophysical Manipulation of the Extracellular Environment by <i>Eurotium halophilicum</i>Anna Micheluz0Flavia Pinzari1Edgard G. Rivera-Valentín2Sabrina Manente3John E. Hallsworth4Conservation Science Department, Deutsches Museum, Museumsinsel 1, 80538 Munich, GermanyInstitute for Biological Systems, Council of National Research of Italy, Area della Ricerca di Roma 1, Via Salaria Km 29,300, 00015 Monterotondo, ItalyJohns Hopkins University Applied Physics Laboratory, Laurel, MD 20723, USADepartment of Molecular Sciences and Nanosystems, Scientific Campus, Ca’ Foscari University of Venice, Via Torino, 30170 Venice, ItalyInstitute for Global Food Security, School of Biological Sciences, Queen’s University Belfast, 19 Chlorine Gardens, Belfast BT9 5DL, UK<i>Eurotium halophilicum</i> 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 <i>E. halophilicum</i> 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 (Na<sub>4</sub>Ca(SO<sub>4</sub>)<sub>3</sub>·2H<sub>2</sub>O) and mirabilite (Na<sub>2</sub>SO<sub>4</sub>·10H<sub>2</sub>O) embedded within extracellular polymeric substances and provide evidence that <i>E. halophilicum</i> 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 <i>E. halophilicum</i> in natural habitats, and the current episode of climate change.https://www.mdpi.com/2076-0817/11/12/1462astrobiologyextracellular polymeric substances (EPS)<i>Eurotium halophilicum</i>global climate changelibrary-book contaminationmodel xerophile species
spellingShingle Anna Micheluz
Flavia Pinzari
Edgard G. Rivera-Valentín
Sabrina Manente
John E. Hallsworth
Biophysical Manipulation of the Extracellular Environment by <i>Eurotium halophilicum</i>
Pathogens
astrobiology
extracellular polymeric substances (EPS)
<i>Eurotium halophilicum</i>
global climate change
library-book contamination
model xerophile species
title Biophysical Manipulation of the Extracellular Environment by <i>Eurotium halophilicum</i>
title_full Biophysical Manipulation of the Extracellular Environment by <i>Eurotium halophilicum</i>
title_fullStr Biophysical Manipulation of the Extracellular Environment by <i>Eurotium halophilicum</i>
title_full_unstemmed Biophysical Manipulation of the Extracellular Environment by <i>Eurotium halophilicum</i>
title_short Biophysical Manipulation of the Extracellular Environment by <i>Eurotium halophilicum</i>
title_sort biophysical manipulation of the extracellular environment by i eurotium halophilicum i
topic astrobiology
extracellular polymeric substances (EPS)
<i>Eurotium halophilicum</i>
global climate change
library-book contamination
model xerophile species
url https://www.mdpi.com/2076-0817/11/12/1462
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