IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42693-6.html
   My bibliography  Save this article

Structural adaptation of fungal cell wall in hypersaline environment

Author

Listed:
  • Liyanage D. Fernando

    (Michigan State University
    University of Georgia)

  • Yordanis Pérez-Llano

    (Universidad Autónoma del Estado de Morelos)

  • Malitha C. Dickwella Widanage

    (Michigan State University
    University of Michigan)

  • Anand Jacob

    (Michigan State University)

  • Liliana Martínez-Ávila

    (Universidad Autónoma del Estado de Morelos)

  • Andrew S. Lipton

    (Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory)

  • Nina Gunde-Cimerman

    (University of Ljubljana)

  • Jean-Paul Latgé

    (University of Crete
    University of Angers)

  • Ramón Alberto Batista-García

    (Universidad Autónoma del Estado de Morelos)

  • Tuo Wang

    (Michigan State University)

Abstract

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.

Suggested Citation

  • Liyanage D. Fernando & Yordanis Pérez-Llano & Malitha C. Dickwella Widanage & Anand Jacob & Liliana Martínez-Ávila & Andrew S. Lipton & Nina Gunde-Cimerman & Jean-Paul Latgé & Ramón Alberto Batista-Ga, 2023. "Structural adaptation of fungal cell wall in hypersaline environment," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42693-6
    DOI: 10.1038/s41467-023-42693-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42693-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-42693-6?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Sonja-Verena Albers, 2016. "Extremophiles: Life at the deep end," Nature, Nature, vol. 538(7626), pages 457-457, October.
    2. Lynn J. Rothschild & Rocco L. Mancinelli, 2001. "Life in extreme environments," Nature, Nature, vol. 409(6823), pages 1092-1101, February.
    3. Arnab Chakraborty & Liyanage D. Fernando & Wenxia Fang & Malitha C. Dickwella Widanage & Pingzhen Wei & Cheng Jin & Thierry Fontaine & Jean-Paul Latgé & Tuo Wang, 2021. "A molecular vision of fungal cell wall organization by functional genomics and solid-state NMR," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    4. Anja Spang & Jimmy H. Saw & Steffen L. Jørgensen & Katarzyna Zaremba-Niedzwiedzka & Joran Martijn & Anders E. Lind & Roel van Eijk & Christa Schleper & Lionel Guy & Thijs J. G. Ettema, 2015. "Complex archaea that bridge the gap between prokaryotes and eukaryotes," Nature, Nature, vol. 521(7551), pages 173-179, May.
    5. Xue Kang & Alex Kirui & Artur Muszyński & Malitha C. Dickwella Widanage & Adrian Chen & Parastoo Azadi & Ping Wang & Frederic Mentink-Vigier & Tuo Wang, 2018. "Molecular architecture of fungal cell walls revealed by solid-state NMR," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Malitha C. Dickwella Widanage & Isha Gautam & Daipayan Sarkar & Frederic Mentink-Vigier & Josh V. Vermaas & Shi-You Ding & Andrew S. Lipton & Thierry Fontaine & Jean-Paul Latgé & Ping Wang & Tuo Wang, 2024. "Adaptative survival of Aspergillus fumigatus to echinocandins arises from cell wall remodeling beyond β−1,3-glucan synthesis inhibition," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Qinghui Cheng & Malitha C. Dickwella Widanage & Jayasubba Reddy Yarava & Ankur Ankur & Jean-Paul Latgé & Ping Wang & Tuo Wang, 2024. "Molecular architecture of chitin and chitosan-dominated cell walls in zygomycetous fungal pathogens by solid-state NMR," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Luis Andrés Yarzábal Rodríguez & Peggy Elizabeth Álvarez Gutiérrez & Nina Gunde-Cimerman & Jimmy Casto Ciancas Jiménez & Adrián Gutiérrez-Cepeda & Ana María Fernández Ocaña & Ramón Alberto Batista-Gar, 2024. "Exploring extremophilic fungi in soil mycobiome for sustainable agriculture amid global change," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Malitha C. Dickwella Widanage & Isha Gautam & Daipayan Sarkar & Frederic Mentink-Vigier & Josh V. Vermaas & Shi-You Ding & Andrew S. Lipton & Thierry Fontaine & Jean-Paul Latgé & Ping Wang & Tuo Wang, 2024. "Adaptative survival of Aspergillus fumigatus to echinocandins arises from cell wall remodeling beyond β−1,3-glucan synthesis inhibition," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Qinghui Cheng & Malitha C. Dickwella Widanage & Jayasubba Reddy Yarava & Ankur Ankur & Jean-Paul Latgé & Ping Wang & Tuo Wang, 2024. "Molecular architecture of chitin and chitosan-dominated cell walls in zygomycetous fungal pathogens by solid-state NMR," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Simona Dzurendova & Boris Zimmermann & Achim Kohler & Valeria Tafintseva & Ondrej Slany & Milan Certik & Volha Shapaval, 2020. "Microcultivation and FTIR spectroscopy-based screening revealed a nutrient-induced co-production of high-value metabolites in oleaginous Mucoromycota fungi," PLOS ONE, Public Library of Science, vol. 15(6), pages 1-34, June.
    4. Jonathan Filée & Hubert F. Becker & Lucille Mellottee & Rima Zein Eddine & Zhihui Li & Wenlu Yin & Jean-Christophe Lambry & Ursula Liebl & Hannu Myllykallio, 2023. "Bacterial origins of thymidylate metabolism in Asgard archaea and Eukarya," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    5. Leonardo Betancurt-Anzola & Markel Martínez-Carranza & Marc Delarue & Kelly M. Zatopek & Andrew F. Gardner & Ludovic Sauguet, 2023. "Molecular basis for proofreading by the unique exonuclease domain of Family-D DNA polymerases," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Silvia Díaz & Ángeles Aguilera & Carolina G. de Figueras & Patricia de Francisco & Sanna Olsson & Fernando Puente-Sánchez & José Eduardo González-Pastor, 2022. "Heterologous Expression of the Phytochelatin Synthase CaPCS2 from Chlamydomonas acidophila and Its Effect on Different Stress Factors in Escherichia coli," IJERPH, MDPI, vol. 19(13), pages 1-21, June.
    7. Yan-Ling Qi & Ya-Ting Chen & Yuan-Guo Xie & Yu-Xian Li & Yang-Zhi Rao & Meng-Meng Li & Qi-Jun Xie & Xing-Ru Cao & Lei Chen & Yan-Ni Qu & Zhen-Xuan Yuan & Zhi-Chao Xiao & Lu Lu & Jian-Yu Jiao & Wen-She, 2024. "Analysis of nearly 3000 archaeal genomes from terrestrial geothermal springs sheds light on interconnected biogeochemical processes," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    8. Louis N. Irwin & Abel Méndez & Alberto G. Fairén & Dirk Schulze-Makuch, 2014. "Assessing the Possibility of Biological Complexity on Other Worlds, with an Estimate of the Occurrence of Complex Life in the Milky Way Galaxy," Challenges, MDPI, vol. 5(1), pages 1-16, May.
    9. Lucas Serra Moncadas & Cyrill Hofer & Paul-Adrian Bulzu & Jakob Pernthaler & Adrian-Stefan Andrei, 2024. "Freshwater genome-reduced bacteria exhibit pervasive episodes of adaptive stasis," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    10. Tara A. Mahendrarajah & Edmund R. R. Moody & Dominik Schrempf & Lénárd L. Szánthó & Nina Dombrowski & Adrián A. Davín & Davide Pisani & Philip C. J. Donoghue & Gergely J. Szöllősi & Tom A. Williams & , 2023. "ATP synthase evolution on a cross-braced dated tree of life," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    11. Zhiguang Qiu & Li Yuan & Chun-Ang Lian & Bin Lin & Jie Chen & Rong Mu & Xuejiao Qiao & Liyu Zhang & Zheng Xu & Lu Fan & Yunzeng Zhang & Shanquan Wang & Junyi Li & Huiluo Cao & Bing Li & Baowei Chen & , 2024. "BASALT refines binning from metagenomic data and increases resolution of genome-resolved metagenomic analysis," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    12. Carolien Bastiaanssen & Pilar Bobadilla Ugarte & Kijun Kim & Giada Finocchio & Yanlei Feng & Todd A. Anzelon & Stephan Köstlbacher & Daniel Tamarit & Thijs J. G. Ettema & Martin Jinek & Ian J. MacRae , 2024. "RNA-guided RNA silencing by an Asgard archaeal Argonaute," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    13. Clément Madru & Markel Martínez-Carranza & Sébastien Laurent & Alessandra C. Alberti & Maelenn Chevreuil & Bertrand Raynal & Ahmed Haouz & Rémy A. Meur & Marc Delarue & Ghislaine Henneke & Didier Flam, 2023. "DNA-binding mechanism and evolution of replication protein A," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    14. Esmeralda Vicedo & Avner Schlessinger & Burkhard Rost, 2015. "Environmental Pressure May Change the Composition Protein Disorder in Prokaryotes," PLOS ONE, Public Library of Science, vol. 10(8), pages 1-21, August.
    15. Ross Corkrey & Tom A McMeekin & John P Bowman & David A Ratkowsky & June Olley & Tom Ross, 2014. "Protein Thermodynamics Can Be Predicted Directly from Biological Growth Rates," PLOS ONE, Public Library of Science, vol. 9(5), pages 1-15, May.
    16. Antonia E Dalziel & Steven Delean & Sarah Heinrich & Phillip Cassey, 2016. "Persistence of Low Pathogenic Influenza A Virus in Water: A Systematic Review and Quantitative Meta-Analysis," PLOS ONE, Public Library of Science, vol. 11(10), pages 1-24, October.
    17. Luís António Menezes Carreira & Dobromir Szadkowski & Stefano Lometto & Georg. K. A. Hochberg & Lotte Søgaard-Andersen, 2023. "Molecular basis and design principles of switchable front-rear polarity and directional migration in Myxococcus xanthus," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    18. Luis E. Valentin-Alvarado & Kathryn E. Appler & Valerie Anda & Marie C. Schoelmerich & Jacob West-Roberts & Veronika Kivenson & Alexander Crits-Christoph & Lynn Ly & Rohan Sachdeva & Chris Greening & , 2024. "Asgard archaea modulate potential methanogenesis substrates in wetland soil," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    19. Guoping Ren & Jie Ye & Qichang Hu & Dong Zhang & Yong Yuan & Shungui Zhou, 2024. "Growth of electroautotrophic microorganisms using hydrovoltaic energy through natural water evaporation," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    20. Liyan Song, 2023. "Toward Understanding Microbial Ecology to Restore a Degraded Ecosystem," IJERPH, MDPI, vol. 20(5), pages 1-9, March.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42693-6. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.