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Title: The obligate alkalophilic soda-lake fungus Sodiomyces alkalinus has shifted to a protein diet

Abstract

Sodiomyces alkalinus is one of the very few alkalophilic fungi, adapted to grow optimally at high pH. It is widely distributed at the plant-deprived edges of extremely alkaline lakes and locally abundant. We sequenced the genome of S. alkalinus and reconstructed evolution of catabolic enzymes, using a phylogenomic comparison. We found that the genome of S. alkalinus is larger, but its predicted proteome is smaller and heavily depleted of both plant-degrading enzymes and proteinases, when compared to its closest plant-pathogenic relatives. Interestingly, despite overall losses, S. alkalinus has retained many proteinases families and acquired bacterial cell wall-degrading enzymes, some of them via horizontal gene transfer from bacteria. This fungus has very potent proteolytic activity at high pH values, but slowly induced low activity of cellulases and hemicellulases. Our experimental and in silico data suggest that plant biomass, a common food source for most fungi, is not a preferred substrate for S. alkalinus in its natural environment. We conclude that the fungus has abandoned the ancestral plant-based diet and has become specialized in a more protein-rich food, abundantly available in soda lakes in the form of prokaryotes and small crustaceans.

Authors:
ORCiD logo [1];  [2];  [1];  [3];  [4];  [4];  [5];  [5];  [1];  [6];  [7];  [8];  [9];  [3];  [5];  [1]
  1. Laboratory of Genetics, Wageningen University, Wageningen The Netherlands
  2. Fungal Physiology, Westerdijk Fungal Biodiversity Institute, Utrecht The Netherlands, R&D Department, Novozymes Latin America, Araucária Paraná Brazil
  3. Laboratory of Phytopathology, Wageningen University, Wageningen The Netherlands
  4. US Department of Energy Joint Genome Institute, Walnut Creek California, Department of Biotechnology, College of Life Sciences and Biotechnology, Korea University, Seoul Korea
  5. US Department of Energy Joint Genome Institute, Walnut Creek California
  6. Centre for Structural and Functional Genomics, Concordia University, Montreal Quebec Canada
  7. Architecture et Fonction des Macromolécules Biologiques, Aix-Marseille University, Marseille France, Institut National de la Recherche Agronomique, USC 1408 AFMB, Marseille France, Department of Biological Sciences, King Abdulaziz University, Jeddah Saudi Arabia
  8. Faculty of Biology, Lomonosov Moscow State University, Moscow Russia
  9. Fungal Physiology, Westerdijk Fungal Biodiversity Institute, Utrecht The Netherlands, Fungal Molecular Physiology, Utrecht University, Utrecht The Netherlands
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1483108
Alternate Identifier(s):
OSTI ID: 1483109; OSTI ID: 1546630
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Published Article
Journal Name:
Molecular Ecology
Additional Journal Information:
Journal Name: Molecular Ecology Journal Volume: 27 Journal Issue: 23; Journal ID: ISSN 0962-1083
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; alkalophilic fungus; brine shrimps; enzymes; HGT; prokaryotes; Sodiomyces alkalinus

Citation Formats

Grum-Grzhimaylo, Alexey A., Falkoski, Daniel L., van den Heuvel, Joost, Valero-Jiménez, Claudio A., Min, Byoungnam, Choi, In-Geol, Lipzen, Anna, Daum, Chris G., Aanen, Duur K., Tsang, Adrian, Henrissat, Bernard, Bilanenko, Elena N., de Vries, Ronald P., van Kan, Jan A. L., Grigoriev, Igor V., and Debets, Alfons J. M. The obligate alkalophilic soda-lake fungus Sodiomyces alkalinus has shifted to a protein diet. United Kingdom: N. p., 2018. Web. doi:10.1111/mec.14912.
Grum-Grzhimaylo, Alexey A., Falkoski, Daniel L., van den Heuvel, Joost, Valero-Jiménez, Claudio A., Min, Byoungnam, Choi, In-Geol, Lipzen, Anna, Daum, Chris G., Aanen, Duur K., Tsang, Adrian, Henrissat, Bernard, Bilanenko, Elena N., de Vries, Ronald P., van Kan, Jan A. L., Grigoriev, Igor V., & Debets, Alfons J. M. The obligate alkalophilic soda-lake fungus Sodiomyces alkalinus has shifted to a protein diet. United Kingdom. doi:10.1111/mec.14912.
Grum-Grzhimaylo, Alexey A., Falkoski, Daniel L., van den Heuvel, Joost, Valero-Jiménez, Claudio A., Min, Byoungnam, Choi, In-Geol, Lipzen, Anna, Daum, Chris G., Aanen, Duur K., Tsang, Adrian, Henrissat, Bernard, Bilanenko, Elena N., de Vries, Ronald P., van Kan, Jan A. L., Grigoriev, Igor V., and Debets, Alfons J. M. Thu . "The obligate alkalophilic soda-lake fungus Sodiomyces alkalinus has shifted to a protein diet". United Kingdom. doi:10.1111/mec.14912.
@article{osti_1483108,
title = {The obligate alkalophilic soda-lake fungus Sodiomyces alkalinus has shifted to a protein diet},
author = {Grum-Grzhimaylo, Alexey A. and Falkoski, Daniel L. and van den Heuvel, Joost and Valero-Jiménez, Claudio A. and Min, Byoungnam and Choi, In-Geol and Lipzen, Anna and Daum, Chris G. and Aanen, Duur K. and Tsang, Adrian and Henrissat, Bernard and Bilanenko, Elena N. and de Vries, Ronald P. and van Kan, Jan A. L. and Grigoriev, Igor V. and Debets, Alfons J. M.},
abstractNote = {Sodiomyces alkalinus is one of the very few alkalophilic fungi, adapted to grow optimally at high pH. It is widely distributed at the plant-deprived edges of extremely alkaline lakes and locally abundant. We sequenced the genome of S. alkalinus and reconstructed evolution of catabolic enzymes, using a phylogenomic comparison. We found that the genome of S. alkalinus is larger, but its predicted proteome is smaller and heavily depleted of both plant-degrading enzymes and proteinases, when compared to its closest plant-pathogenic relatives. Interestingly, despite overall losses, S. alkalinus has retained many proteinases families and acquired bacterial cell wall-degrading enzymes, some of them via horizontal gene transfer from bacteria. This fungus has very potent proteolytic activity at high pH values, but slowly induced low activity of cellulases and hemicellulases. Our experimental and in silico data suggest that plant biomass, a common food source for most fungi, is not a preferred substrate for S. alkalinus in its natural environment. We conclude that the fungus has abandoned the ancestral plant-based diet and has become specialized in a more protein-rich food, abundantly available in soda lakes in the form of prokaryotes and small crustaceans.},
doi = {10.1111/mec.14912},
journal = {Molecular Ecology},
number = 23,
volume = 27,
place = {United Kingdom},
year = {2018},
month = {11}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1111/mec.14912

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