Structural adaptation of fungal cell wall in hypersaline environment

Fernando, Liyanage D.; Pérez-Llano, Yordanis; Dickwella Widanage, Malitha C.; Jacob, Anand; Martínez-Ávila, Liliana; Lipton, Andrew S.; Gunde-Cimerman, Nina; Latgé, Jean-Paul; Batista-García, Ramón Alberto; Wang, Tuo

doi:10.1038/s41467-023-42693-6

Title: Structural adaptation of fungal cell wall in hypersaline environment

Journal Article · 04 November 2023 · Nature Communications

DOI: https://doi.org/10.1038/s41467-023-42693-6 · OSTI ID:2204730

Fernando, Liyanage D. ^[1];

^[2]; Dickwella Widanage, Malitha C. ^[3]; Jacob, Anand ^[4];

^[2];

^[5];

^[6]; Latgé, Jean-Paul ^[7];

^[2];

^[4]

Univ. of Georgia, Athens, GA (United States); Michigan State Univ., East Lansing, MI (United States)
Universidad Autónoma del Estado de Morelos, Cuernavaca (Mexico)
Univ. of Michigan, Ann Arbor, MI (United States); Michigan State Univ., East Lansing, MI (United States)
Michigan State Univ., East Lansing, MI (United States)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Univ. of Ljubljana (Slovenia)
Univ. of Crete, Heraklion (Greece); University of Angers (France)

Halophilic fungi thrive in hypersaline habitats and face a range of extreme conditions. These fungal species have gained considerable attention due to their potential applications in harsh industrial processes, such as bioremediation and fermentation under unfavorable conditions of hypersalinity, low water activity, and extreme pH. However, the role of the cell wall in surviving these environmental conditions remains unclear. Here we employ solid-state NMR spectroscopy to compare the cell wall architecture of Aspergillus sydowii across salinity gradients. Analyses of intact cells reveal that A. sydowii cell walls contain a rigid core comprising chitin, β-glucan, and chitosan, shielded by a surface shell composed of galactomannan and galactosaminogalactan. When exposed to hypersaline conditions, A. sydowii enhances chitin biosynthesis and incorporates α-glucan to create thick, stiff, and hydrophobic cell walls. Such structural rearrangements enable the fungus to adapt to both hypersaline and salt-deprived conditions, providing a robust mechanism for withstanding external stress. These molecular principles can aid in the optimization of halophilic strains for biotechnology applications.

View Journal Article

Cite

Export

Save

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); USDOE

Grant/Contract Number:: AC05-76RL01830; AI173270

OSTI ID:: 2204730

Alternate ID(s):: OSTI ID: 2328593

Report Number(s):: PNNL-SA-193998

Journal Information:: Nature Communications, Vol. 14, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (83)

Hidden motions and motion-induced invisibility: Dynamics-based spectral editing in solid-state NMR Matlahov, Irina; van der Wel, Patrick C. A. Methods, Vol. 148 https://doi.org/10.1016/j.ymeth.2018.04.015	journal	September 2018
Galactofuranose containing molecules in Aspergillus fumigatus Latge, Jean-Paul Medical Mycology, Vol. 47, Issue s1 https://doi.org/10.1080/13693780802258832	journal	January 2009
Galactomannan Produced by Aspergillus fumigatus: An Update on the Structure, Biosynthesis and Biological Functions of an Emblematic Fungal Biomarker Fontaine, Thierry; Latgé, Jean-Paul Journal of Fungi, Vol. 6, Issue 4 https://doi.org/10.3390/jof6040283	journal	November 2020
Solid-state NMR spectroscopy Reif, Bernd; Ashbrook, Sharon E.; Emsley, Lyndon Nature Reviews Methods Primers, Vol. 1, Issue 1 https://doi.org/10.1038/s43586-020-00002-1	journal	January 2021
Phylogeny of xerophilic aspergilli (subgenus Aspergillus) and taxonomic revision of section Restricti Sklenář, F.; Jurjević, Ž.; Zalar, P. Studies in Mycology, Vol. 88 https://doi.org/10.1016/j.simyco.2017.09.002	journal	September 2017
Stress Reshapes the Physiological Response of Halophile Fungi to Salinity Pérez-Llano, Yordanis; Rodríguez-Pupo, Eya Caridad; Druzhinina, Irina S. Cells, Vol. 9, Issue 3 https://doi.org/10.3390/cells9030525	journal	February 2020
Water–Polysaccharide Interactions in the Primary Cell Wall of Arabidopsis thaliana from Polarization Transfer Solid-State NMR White, Paul B.; Wang, Tuo; Park, Yong Bum Journal of the American Chemical Society, Vol. 136, Issue 29 https://doi.org/10.1021/ja504108h	journal	July 2014
Aspergillus sydowii and Other Potential Fungal Pathogens in Gorgonian Octocorals of the Ecuadorian Pacific Soler-Hurtado, M. Mar; Sandoval-Sierra, José Vladimir; Machordom, Annie PLOS ONE, Vol. 11, Issue 11 https://doi.org/10.1371/journal.pone.0165992	journal	November 2016
Strategies of adaptation of microorganisms of the three domains of life to high salt concentrations Gunde-Cimerman, Nina; Plemenitaš, Ana; Oren, Aharon FEMS Microbiology Reviews, Vol. 42, Issue 3 https://doi.org/10.1093/femsre/fuy009	journal	February 2018
First demonstration that ascomycetous halophilic fungi (Aspergillus sydowii and Aspergillus destruens) are useful in xenobiotic mycoremediation under high salinity conditions González-Abradelo, Deborah; Pérez-Llano, Yordanis; Peidro-Guzmán, Heidy Bioresource Technology, Vol. 279 https://doi.org/10.1016/j.biortech.2019.02.002	journal	May 2019
Morphological Response of the Halophilic Fungal Genus Wallemia to High Salinity Kralj Kunčič, Marjetka; Kogej, Tina; Drobne, Damjana Applied and Environmental Microbiology, Vol. 76, Issue 1 https://doi.org/10.1128/AEM.02318-09	journal	January 2010
Chitinases and Peptide Mimotopes Beauvais, Anne; Latgé, Jean-Paul Chemistry & Biology, Vol. 12, Issue 1 https://doi.org/10.1016/j.chembiol.2005.01.001	journal	January 2005
Identifying candidate Aspergillus pathogenicity factors by annotation frequency Pennerman, Kayla K.; Yin, Guohua; Glenn, Anthony E. BMC Microbiology, Vol. 20, Issue 1 https://doi.org/10.1186/s12866-020-02031-y	journal	November 2020
The Fungal Cell Wall: Structure, Biosynthesis, and Function Gow, Neil A. R.; Latge, Jean-Paul; Munro, Carol A. Microbiology Spectrum, Vol. 5, Issue 3 https://doi.org/10.1128/microbiolspec.FUNK-0035-2016	journal	June 2017
Galactosaminogalactan (GAG) and its multiple roles in Aspergillus pathogenesis Speth, Cornelia; Rambach, Günter; Lass-Flörl, Cornelia Virulence, Vol. 10, Issue 1 https://doi.org/10.1080/21505594.2019.1568174	journal	January 2019
Structural Rearrangements of Membrane Proteins Probed by Water-Edited Solid-State NMR Spectroscopy Ader, Christian; Schneider, Robert; Seidel, Karsten Journal of the American Chemical Society, Vol. 131, Issue 1 https://doi.org/10.1021/ja806306e	journal	January 2009
Structural Polymorphism of Chitin and Chitosan in Fungal Cell Walls From Solid-State NMR and Principal Component Analysis Fernando, Liyanage D.; Dickwella Widanage, Malitha C.; Penfield, Jackson Frontiers in Molecular Biosciences, Vol. 8 https://doi.org/10.3389/fmolb.2021.727053	journal	August 2021
Molecular Organization of the Alkali-insoluble Fraction ofAspergillus fumigatus Cell Wall Fontaine, Thierry; Simenel, Catherine; Dubreucq, Guy Journal of Biological Chemistry, Vol. 275, Issue 36 https://doi.org/10.1074/jbc.M909975199	journal	September 2000
Genome and transcriptome sequencing of the halophilic fungus Wallemia ichthyophaga: haloadaptations present and absent Zajc, Janja; Liu, Yongfeng; Dai, Wenkui BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-617	journal	January 2013
Integrative Model of Oxidative Stress Adaptation in the Fungal Pathogen Candida albicans Komalapriya, Chandrasekaran; Kaloriti, Despoina; Tillmann, Anna T. PLOS ONE, Vol. 10, Issue 9 https://doi.org/10.1371/journal.pone.0137750	journal	September 2015
Aspergillus atacamensis and A. salisburgensis: two new halophilic species from hypersaline/arid habitats with a phialosimplex-like morphology Martinelli, Livia; Zalar, Polona; Gunde-Cimerman, Nina Extremophiles, Vol. 21, Issue 4 https://doi.org/10.1007/s00792-017-0941-3	journal	May 2017
Solid-state NMR of plant and fungal cell walls: A critical review Zhao, Wancheng; Fernando, Liyanage D.; Kirui, Alex Solid State Nuclear Magnetic Resonance, Vol. 107 https://doi.org/10.1016/j.ssnmr.2020.101660	journal	June 2020
Solid-state NMR molecular snapshots of Aspergillus fumigatus cell wall architecture during a conidial morphotype transition Lamon, Gaëlle; Lends, Alons; Valsecchi, Isabel Proceedings of the National Academy of Sciences, Vol. 120, Issue 6 https://doi.org/10.1073/pnas.2212003120	journal	January 2023
Halotolerant and halophilic fungi Gunde-Cimerman, Nina; Ramos, Jose; Plemenitaš, Ana Mycological Research, Vol. 113, Issue 11 https://doi.org/10.1016/j.mycres.2009.09.002	journal	November 2009
Adaptation of Candida albicans to environmental pH induces cell wall remodelling and enhances innate immune recognition Sherrington, Sarah L.; Sorsby, Eleanor; Mahtey, Nabeel PLOS Pathogens, Vol. 13, Issue 5 https://doi.org/10.1371/journal.ppat.1006403	journal	May 2017
Aspergillus Galactosaminogalactan Mediates Adherence to Host Constituents and Conceals Hyphal β-Glucan from the Immune System Gravelat, Fabrice N.; Beauvais, Anne; Liu, Hong PLoS Pathogens, Vol. 9, Issue 8 https://doi.org/10.1371/journal.ppat.1003575	journal	August 2013
1H-detected characterization of carbon–carbon networks in highly flexible protonated biomolecules using MAS NMR Bahri, Salima; Safeer, Adil; Adler, Agnes Journal of Biomolecular NMR, Vol. 77, Issue 3 https://doi.org/10.1007/s10858-023-00415-6	journal	June 2023
Extremophiles: Life at the deep end Albers, Sonja-Verena Nature, Vol. 538, Issue 7626 https://doi.org/10.1038/538457a	journal	October 2016
Haloadaptative Responses of Aspergillus sydowii to Extreme Water Deprivation: Morphology, Compatible Solutes, and Oxidative Stress at NaCl Saturation Jiménez-Gómez, Irina; Valdés-Muñoz, Gisell; Moreno-Perlin, Tonatiuh Journal of Fungi, Vol. 6, Issue 4 https://doi.org/10.3390/jof6040316	journal	November 2020
Osmolyte Signatures for the Protection of Aspergillus sydowii Cells under Halophilic Conditions and Osmotic Shock Rodríguez-Pupo, Eya Caridad; Pérez-Llano, Yordanis; Tinoco-Valencia, José Raunel Journal of Fungi, Vol. 7, Issue 6 https://doi.org/10.3390/jof7060414	journal	May 2021
Biotechnological Applications of Halophilic Fungi: Past, Present, and Future Ali, Imran; Khaliq, Samira; Sajid, Sumbal Fungi in Extreme Environments: Ecological Role and Biotechnological Significance https://doi.org/10.1007/978-3-030-19030-9_15	book	January 2019
Histoplasma capsulatum -(1,3)-glucan blocks innate immune recognition by the beta-glucan receptor Rappleye, C. A.; Eissenberg, L. G.; Goldman, W. E. Proceedings of the National Academy of Sciences, Vol. 104, Issue 4 https://doi.org/10.1073/pnas.0609848104	journal	January 2007
CCMRD: a solid-state NMR database for complex carbohydrates Kang, Xue; Zhao, Wancheng; Dickwella Widanage, Malitha C. Journal of Biomolecular NMR, Vol. 74, Issue 4-5 https://doi.org/10.1007/s10858-020-00304-2	journal	March 2020
Osmoadaptation Strategy of the Most Halophilic Fungus, Wallemia ichthyophaga, Growing Optimally at Salinities above 15% NaCl Zajc, Janja; Kogej, Tina; Galinski, Erwin A. Applied and Environmental Microbiology, Vol. 80, Issue 1 https://doi.org/10.1128/AEM.02702-13	journal	January 2014
Characterization of Lignocellulolytic Activities from a Moderate Halophile Strain of Aspergillus caesiellus Isolated from a Sugarcane Bagasse Fermentation Batista-García, Ramón Alberto; Balcázar-López, Edgar; Miranda-Miranda, Estefan PLoS ONE, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pone.0105893	journal	August 2014
A molecular vision of fungal cell wall organization by functional genomics and solid-state NMR Chakraborty, Arnab; Fernando, Liyanage D.; Fang, Wenxia Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-26749-z	journal	November 2021
Glycosylphosphatidylinositol-anchored Glucanosyltransferases Play an Active Role in the Biosynthesis of the Fungal Cell Wall Mouyna, Isabelle; Fontaine, Thierry; Vai, Marina Journal of Biological Chemistry, Vol. 275, Issue 20 https://doi.org/10.1074/jbc.275.20.14882	journal	May 2000
Hydrophobins: multifunctional biosurfactants for interface engineering Berger, Bryan W.; Sallada, Nathanael D. Journal of Biological Engineering, Vol. 13, Issue 1 https://doi.org/10.1186/s13036-018-0136-1	journal	January 2019
Extremophiles as a source for novel enzymes van den Burg, Bertus Current Opinion in Microbiology, Vol. 6, Issue 3 https://doi.org/10.1016/S1369-5274(03)00060-2	journal	June 2003
Architecture of the dynamic fungal cell wall Gow, Neil A. R.; Lenardon, Megan D. Nature Reviews Microbiology, Vol. 21, Issue 4 https://doi.org/10.1038/s41579-022-00796-9	journal	October 2022
High-resolution solid-state carbon-13 nuclear magnetic resonance study of chitin Tanner, Steven F.; Chanzy, Henri; Vincendon, Marc Macromolecules, Vol. 23, Issue 15 https://doi.org/10.1021/ma00217a008	journal	July 1990
The Cell Wall of the Human Fungal Pathogen Aspergillus fumigatus : Biosynthesis, Organization, Immune Response, and Virulence Latgé, Jean-Paul; Beauvais, Anne; Chamilos, Georgios Annual Review of Microbiology, Vol. 71, Issue 1 https://doi.org/10.1146/annurev-micro-030117-020406	journal	September 2017
Modern Biophysics Redefines Our Understanding of Fungal Cell Wall Structure, Complexity, and Dynamics Latgé, Jean-Paul; Wang, Tuo mBio, Vol. 13, Issue 3 https://doi.org/10.1128/mbio.01145-22	journal	June 2022
Investigation of Dipolar-Mediated Water−Protein Interactions in Microcrystalline Crh by Solid-State NMR Spectroscopy Lesage, Anne; Emsley, Lyndon; Penin, François Journal of the American Chemical Society, Vol. 128, Issue 25 https://doi.org/10.1021/ja060866q	journal	June 2006
Characterization of the cell wall of a mushroom forming fungus at atomic resolution using solid-state NMR spectroscopy Ehren, Helena Leona; Appels, Freek V. W.; Houben, Klaartje The Cell Surface, Vol. 6 https://doi.org/10.1016/j.tcsw.2020.100046	journal	December 2020
Genomic adaptations of the halophilic Dead Sea filamentous fungus Eurotium rubrum Kis-Papo, Tamar; Weig, Alfons R.; Riley, Robert Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4745	journal	May 2014
Transcriptomic analysis of polyaromatic hydrocarbon degradation by the halophilic fungus Aspergillus sydowii at hypersaline conditions Peidro‐Guzmán, Heidy; Pérez‐Llano, Yordanis; González‐Abradelo, Deborah Environmental Microbiology, Vol. 23, Issue 7 https://doi.org/10.1111/1462-2920.15166	journal	August 2020
Characterization of Aspergillus sydowii (Thom et Church), a fungal pathogen of Caribbean sea fan corals Alker, Alisa P.; Smith, Garriet W.; Kim, Kiho Hydrobiologia, Vol. 460, Issue 1/3, p. 105-111 https://doi.org/10.1023/A:1013145524136	journal	September 2001
Halophiles and their enzymes: negativity put to good use DasSarma, Shiladitya; DasSarma, Priya Current Opinion in Microbiology, Vol. 25 https://doi.org/10.1016/j.mib.2015.05.009	journal	June 2015
Back to the Salt Mines: Genome and Transcriptome Comparisons of the Halophilic Fungus Aspergillus salisburgensis and Its Halotolerant Relative Aspergillus sclerotialis Tafer, Hakim; Poyntner, Caroline; Lopandic, Ksenija Genes, Vol. 10, Issue 5 https://doi.org/10.3390/genes10050381	journal	May 2019
Mild Heat Stress Affects on the Cell Wall Structure in Candida albicans Biofilm Ikezaki, Shojiro; Cho, Tamaki; Nagao, Jun-ichi Medical Mycology Journal, Vol. 60, Issue 2 https://doi.org/10.3314/mmj.19-00001	journal	January 2019
Life in extreme environments Rothschild, Lynn J.; Mancinelli, Rocco L. Nature, Vol. 409, Issue 6823 https://doi.org/10.1038/35059215	journal	February 2001
Molecular architecture of fungal cell walls revealed by solid-state NMR Kang, Xue; Kirui, Alex; Muszyński, Artur Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05199-0	journal	July 2018
High-resolution solid-state carbon-13 NMR study of chitosan and its salts with acids: conformational characterization of polymorphs and helical structures as viewed from the conformation-dependent carbon-13 chemical shifts Saito, Hajime; Tabeta, Ryoko; Ogawa, Kozo Macromolecules, Vol. 20, Issue 10 https://doi.org/10.1021/ma00176a017	journal	October 1987
The Dual Activity Responsible for the Elongation and Branching of β-(1,3)-Glucan in the Fungal Cell Wall Aimanianda, Vishukumar; Simenel, Catherine; Garnaud, Cecile mBio, Vol. 8, Issue 3 https://doi.org/10.1128/mBio.00619-17	journal	July 2017
Tailoring NMR experiments for structural characterization of amorphous biological solids: A practical guide Kelly, John E.; Chrissian, Christine; Stark, Ruth E. Solid State Nuclear Magnetic Resonance, Vol. 109 https://doi.org/10.1016/j.ssnmr.2020.101686	journal	October 2020
Deletion of the α-(1,3)-Glucan Synthase Genes Induces a Restructuring of the Conidial Cell Wall Responsible for the Avirulence of Aspergillus fumigatus Beauvais, Anne; Bozza, Silvia; Kniemeyer, Olaf PLoS Pathogens, Vol. 9, Issue 11 https://doi.org/10.1371/journal.ppat.1003716	journal	November 2013
Hydrophobins—Unique Fungal Proteins Bayry, Jagadeesh; Aimanianda, Vishukumar; Guijarro, J. Iñaki PLoS Pathogens, Vol. 8, Issue 5 https://doi.org/10.1371/journal.ppat.1002700	journal	May 2012
Understanding Aspergillus fumigatus galactosaminogalactan biosynthesis: A few questions remain Le Mauff, François; Sheppard, Donald C. The Cell Surface, Vol. 9 https://doi.org/10.1016/j.tcsw.2023.100095	journal	December 2023
What Are the Functions of Chitin Deacetylases in Aspergillus fumigatus? Mouyna, Isabelle; Dellière, Sarah; Beauvais, Anne Frontiers in Cellular and Infection Microbiology, Vol. 10 https://doi.org/10.3389/fcimb.2020.00028	journal	February 2020
Galactosaminogalactan activates the inflammasome to provide host protection Briard, Benoit; Fontaine, Thierry; Samir, Parimal Nature, Vol. 588, Issue 7839 https://doi.org/10.1038/s41586-020-2996-z	journal	December 2020
Through-Bond Carbon−Carbon Connectivities in Disordered Solids by NMR Lesage, Anne; Bardet, Michel; Emsley, Lyndon Journal of the American Chemical Society, Vol. 121, Issue 47 https://doi.org/10.1021/ja992272b	journal	December 1999
Molecular insights into the complex mechanics of plant epidermal cell walls Zhang, Yao; Yu, Jingyi; Wang, Xuan Science, Vol. 372, Issue 6543 https://doi.org/10.1126/science.abf2824	journal	May 2021
Solid-state NMR spectroscopy identifies three classes of lipids in Cryptococcus neoformans melanized cell walls and whole fungal cells Chrissian, Christine; Camacho, Emma; Kelly, John E. Journal of Biological Chemistry, Vol. 295, Issue 44 https://doi.org/10.1074/jbc.RA120.015201	journal	August 2020
Complex archaea that bridge the gap between prokaryotes and eukaryotes Spang, Anja; Saw, Jimmy H.; Jørgensen, Steffen L. Nature, Vol. 521, Issue 7551 https://doi.org/10.1038/nature14447	journal	May 2015
In-Cell Solid-State NMR: An Emerging Technique for the Study of Biological Membranes Warnet, Xavier L.; Arnold, Alexandre A.; Marcotte, Isabelle Biophysical Journal, Vol. 109, Issue 12 https://doi.org/10.1016/j.bpj.2015.10.041	journal	December 2015
Enzymes of UDP-GlcNAc biosynthesis in yeast Milewski, Sławomir; Gabriel, Iwona; Olchowy, Jarosław Yeast, Vol. 23, Issue 1 https://doi.org/10.1002/yea.1337	journal	January 2006
Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus de Vries, Ronald P.; Riley, Robert; Wiebenga, Ad Genome Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s13059-017-1151-0	journal	February 2017
The cell wall: a carbohydrate armour for the fungal cell Latgé, Jean-Paul Molecular Microbiology, Vol. 66, Issue 2 https://doi.org/10.1111/j.1365-2958.2007.05872.x	journal	October 2007
Secondary and Tertiary Structural Effects on Protein NMR Chemical Shifts: an ab Initio Approach de Dios, Angel C.; Pearson, John G.; Oldfield, Eric Science, Vol. 260, Issue 5113 https://doi.org/10.1126/science.8502992	journal	June 1993
Direct observation of hierarchical protein dynamics Lewandowski, J. R.; Halse, M. E.; Blackledge, M. Science, Vol. 348, Issue 6234 https://doi.org/10.1126/science.aaa6111	journal	April 2015
Broadband homonuclear correlation spectroscopy driven by combined R2nv sequences under fast magic angle spinning for NMR structural analysis of organic and biological solids Hou, Guangjin; Yan, Si; Trébosc, Julien Journal of Magnetic Resonance, Vol. 232 https://doi.org/10.1016/j.jmr.2013.04.009	journal	July 2013
Osmotic adaptation of the halophilic fungus Hortaea werneckii: role of osmolytes and melanization Kogej, Tina; Stein, Marlene; Volkmann, Marc Microbiology, Vol. 153, Issue 12 https://doi.org/10.1099/mic.0.2007/010751-0	journal	December 2007
Living at the Extremes: Extremophiles and the Limits of Life in a Planetary Context Merino, Nancy; Aronson, Heidi S.; Bojanova, Diana P. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00780	journal	April 2019
Recent advances in the understanding of the Aspergillus fumigatus cell wall Lee, Mark J.; Sheppard, Donald C. Journal of Microbiology, Vol. 54, Issue 3 https://doi.org/10.1007/s12275-016-6045-4	journal	February 2016
Proton to Carbon-13 INEPT in Solid-State NMR Spectroscopy Elena, Bénédicte; Lesage, Anne; Steuernagel, Stefan Journal of the American Chemical Society, Vol. 127, Issue 49 https://doi.org/10.1021/ja054411x	journal	December 2005
The Glycosylphosphatidylinositol-Anchored DFG Family Is Essential for the Insertion of Galactomannan into the β-(1,3)-Glucan–Chitin Core of the Cell Wall of Aspergillus fumigatus Muszkieta, Laetitia; Fontaine, Thierry; Beau, Rémi mSphere, Vol. 4, Issue 4 https://doi.org/10.1128/mSphere.00397-19	journal	August 2019
Solid-State NMR Investigations of Extracellular Matrixes and Cell Walls of Algae, Bacteria, Fungi, and Plants Ghassemi, Nader; Poulhazan, Alexandre; Deligey, Fabien Chemical Reviews https://doi.org/10.1021/acs.chemrev.1c00669	journal	December 2021
Deciphering the role of the chitin synthase families 1 and 2 in the in vivo and in vitro growth of A spergillus fumigatus by multiple gene targeting deletion: Family 1 and 2 chitin synthases in Aspergillus fumigatus Muszkieta, Laetitia; Aimanianda, Vishukumar; Mellado, Emilia Cellular Microbiology, Vol. 16, Issue 12 https://doi.org/10.1111/cmi.12326	journal	August 2014
α- and β-1,3-Glucan Synthesis and Remodeling Wagener, Johannes; Striegler, Kristina; Wagener, Nikola Current Topics in Microbiology and Immunology https://doi.org/10.1007/82_2020_200	book	January 2020
Probing Cell‐Surface Interactions in Fungal Cell Walls by High‐Resolution ¹H‐Detected Solid‐State NMR Spectroscopy Safeer, Adil; Kleijburg, Fleur; Bahri, Salima Chemistry – A European Journal, Vol. 29, Issue 1 https://doi.org/10.1002/chem.202202616	journal	November 2022
Structural Adaptation of Fungal Cell Wall in Hypersaline Environment Fernando, Liyanage D.; Pérez-Llano, Yordanis; Dickwella Widanage, Malitha Zenodo https://doi.org/10.5281/zenodo.10001628	dataset	January 2023
Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus Vries, Ronald De; Riley, Robert; Wiebenga, Ad Figshare https://doi.org/10.6084/m9.figshare.c.3691663	collection	January 2017