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Chrissian C, Lin CP, Camacho E, Casadevall A, Neiman AM, Stark RE
Unconventional constituents and shared molecular architecture of the melanized cell wall of C. neoformans and spore wall of S. cerevisiae
Journal of Fungi 6(4) (2020)
ID 329
Saccharomyces cerevisiae AN120
(Ancestor NCBI TaxID 4932,
species name lookup)
Cryptococcus neoformans H99
(later renamed to: Cryptococcus neoformans var. grubii H99)
(NCBI TaxID 235443,
species name lookup)
Taxonomic group: fungi / Ascomycota, Basidiomycota
(Phylum: Ascomycota, Basidiomycota)
Organ / tissue: cell wallAssociated disease: infection due to Cryptococcus neoformans [ICD11:
XN3EH 
]
NCBI PubMed ID: 33271921Publication DOI: 10.3390/jof6040329Journal NLM ID: 101671827Publisher: Basel, Switzerland: MDPI AG
Correspondence: Neiman AM <aaron.neiman
stonybrook.edu>; Stark RE <rstark
ccny.cuny.edu>
Institutions: Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, Johns Hopkins University, Baltimore, USA, CUNY Institute for Macromolecular Assemblies, City University of New York, New York, NY, USA, Department of Chemistry and Biochemistry, The City College of New York, New York, USA, Ph.D. Program in Biochemistry, The Graduate Center of the City University of New York, New York, NY, USA, Department of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, USA
The fungal cell wall serves as the interface between the cell and the environment. Fungal cell walls are composed largely of polysaccharides, primarily glucans and chitin, though in many fungi stress-resistant cell types elaborate additional cell wall structures. Here, we use solid-state nuclear magnetic resonance spectroscopy to compare the architecture of cell wall fractions isolated from Saccharomyces cerevisiae spores and Cryptococcus neoformans melanized cells. The specialized cell walls of these two divergent fungi are highly similar in composition. Both use chitosan, the deacetylated derivative of chitin, as a scaffold on which a polyaromatic polymer, dityrosine and melanin, respectively, is assembled. Additionally, we demonstrate that a previously identified but uncharacterized component of the S. cerevisiae spore wall is composed of triglycerides, which are also present in the C. neoformans melanized cell wall. Moreover, we identify a tyrosine-derived constituent in the C. neoformans wall that, although it is not dityrosine, is a non-pigment constituent of the cell wall. The similar composition of the walls of these two phylogenetically distant species suggests that triglycerides, polyaromatics, and chitosan are basic building blocks used to assemble highly stress-resistant cell walls and the use of these constituents may be broadly conserved in other fungal species.
chitosan, Saccharomyces cerevisiae, chitin, fungal cell wall, solid-state NMR, Cryptococcus neoformans, melanin, macromolecular assembly, dityrosine, triglycerides
Structure type: homopolymer
Location inside paper: Fig. 2, chitin
Trivial name: chitin
Compound class: O-polysaccharide, cell wall polysaccharide, glucan, polysaccharide, chitin
Contained glycoepitopes: IEDB_135813,IEDB_137340,IEDB_141807,IEDB_151531,IEDB_153212,IEDB_241099,IEDB_423114,IEDB_423150,SB_74,SB_85
Methods: enzymatic digestion, hydrolysis, isotopic labeling, cell growth, delipidation, centrifugation, 13C CPMAS NMR, 13C-13C DARR NMR
Related record ID(s): 40760, 40800, 41831, 49862, 50302, 50305, 50306, 50310, 50312, 50313, 50316, 50318, 111874, 121703, 131817, 139821, 143656, 147987, 149876
NCBI Taxonomy refs (TaxIDs): 4932,
235443Reference(s) to other database(s): GTC:G97099AY, CCSD:
46067, CBank-STR:5851, GenDB:KF905651
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Chrissian C, Lin CP, Camacho E, Casadevall A, Neiman AM, Stark RE
Unconventional constituents and shared molecular architecture of the melanized cell wall of C. neoformans and spore wall of S. cerevisiae
Journal of Fungi 6(4) (2020)
ID 329
Saccharomyces cerevisiae AN120
(Ancestor NCBI TaxID 4932,
species name lookup)
Cryptococcus neoformans H99
(later renamed to: Cryptococcus neoformans var. grubii H99)
(NCBI TaxID 235443,
species name lookup)
Taxonomic group: fungi / Ascomycota, Basidiomycota
(Phylum: Ascomycota, Basidiomycota)
Organ / tissue: cell wallAssociated disease: infection due to Cryptococcus neoformans [ICD11:
XN3EH ]
NCBI PubMed ID: 33271921Publication DOI: 10.3390/jof6040329Journal NLM ID: 101671827Publisher: Basel, Switzerland: MDPI AG
Correspondence: Neiman AM <aaron.neiman
stonybrook.edu>; Stark RE <rstark
ccny.cuny.edu>
Institutions: Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, Johns Hopkins University, Baltimore, USA, CUNY Institute for Macromolecular Assemblies, City University of New York, New York, NY, USA, Department of Chemistry and Biochemistry, The City College of New York, New York, USA, Ph.D. Program in Biochemistry, The Graduate Center of the City University of New York, New York, NY, USA, Department of Biochemistry and Cell Biology, Stony Brook University, Stony Brook, USA
The fungal cell wall serves as the interface between the cell and the environment. Fungal cell walls are composed largely of polysaccharides, primarily glucans and chitin, though in many fungi stress-resistant cell types elaborate additional cell wall structures. Here, we use solid-state nuclear magnetic resonance spectroscopy to compare the architecture of cell wall fractions isolated from Saccharomyces cerevisiae spores and Cryptococcus neoformans melanized cells. The specialized cell walls of these two divergent fungi are highly similar in composition. Both use chitosan, the deacetylated derivative of chitin, as a scaffold on which a polyaromatic polymer, dityrosine and melanin, respectively, is assembled. Additionally, we demonstrate that a previously identified but uncharacterized component of the S. cerevisiae spore wall is composed of triglycerides, which are also present in the C. neoformans melanized cell wall. Moreover, we identify a tyrosine-derived constituent in the C. neoformans wall that, although it is not dityrosine, is a non-pigment constituent of the cell wall. The similar composition of the walls of these two phylogenetically distant species suggests that triglycerides, polyaromatics, and chitosan are basic building blocks used to assemble highly stress-resistant cell walls and the use of these constituents may be broadly conserved in other fungal species.
chitosan, Saccharomyces cerevisiae, chitin, fungal cell wall, solid-state NMR, Cryptococcus neoformans, melanin, macromolecular assembly, dityrosine, triglycerides
Structure type: structural motif or average structure
Location inside paper: Fig. 2, chitosan
Trivial name: chitosan
Compound class: O-polysaccharide, cell wall polysaccharide, glucan, polysaccharide
Contained glycoepitopes: IEDB_135813,IEDB_137340,IEDB_141807,IEDB_151531,IEDB_153212,IEDB_241099,IEDB_423114,IEDB_423150,SB_74,SB_85
Methods: enzymatic digestion, hydrolysis, isotopic labeling, cell growth, delipidation, centrifugation, 13C CPMAS NMR, 13C-13C DARR NMR
Related record ID(s): 41553, 44877, 44886, 46311, 46570, 46683, 48760, 48774, 49133, 49502, 49512, 49524, 49653, 50016, 50301, 50303, 50304, 50307, 50308, 50309, 50311, 50314, 50315, 50317, 50319, 50320
NCBI Taxonomy refs (TaxIDs): 4932,
235443Reference(s) to other database(s): GTC:G97099AY
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There is only one chemically distinct structure:
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Chrissian C, Camacho E, Fu MS, Prados-Rosales R, Chatterjee S, Cordero RJB, Lodge JK, Casadevall A, Stark RE
Melanin deposition in two Cryptococcus species depends on cell-wall composition and flexibility
Journal of Biological Chemistry 295(7) (2020)
1815-1828
Cryptococcus neoformans H99
(later renamed to: Cryptococcus neoformans var. grubii H99)
(NCBI TaxID 235443,
species name lookup)
Cryptococcus neoformans ST211A
(Ancestor NCBI TaxID 5207,
species name lookup)
Cryptococcus gattii R265
(later renamed to: Cryptococcus gattii VGII R265)
(NCBI TaxID 294750,
species name lookup)
Cryptococcus gattii Cg53
(later renamed to: Cryptococcus gattii VGI Cg53)
(Ancestor NCBI TaxID 37769,
species name lookup)
Taxonomic group: fungi / Basidiomycota
(Phylum: Basidiomycota)
Organ / tissue: cell wallAssociated disease: infection due to Cryptococcus neoformans [ICD11:
XN3EH ];
infection due to Cryptococcus gattii [ICD11:
XN0LE ]
NCBI PubMed ID: 31896575Publication DOI: 10.1074/jbc.RA119.011949Journal NLM ID: 2985121RPublisher: Baltimore, MD: American Society for Biochemistry and Molecular Biology
Correspondence: rstark
ccny.cuny.edu
Institutions: Department of Preventive Medicine and Public Health and Microbiology, Autonoma University of Madrid, Madrid, Spain, Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, USA, Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, Johns Hopkins University, Baltimore, USA, Ph.D. Program in Biochemistry, The Graduate Center of the City University of New York, New York, NY, USA, Department of Chemistry and Biochemistry, City College of New York and CUNY Institute for Macromolecular Assemblies, New York, USA, Department of Microbiology and Immunology, Albert Einstein College of Medicine, Yeshiva University, Bronx, USA
Cryptococcus neoformans and Cryptococcus gattii are two species complexes in the large fungal genus Cryptococcus and are responsible for potentially lethal disseminated infections. These two complexes share several phenotypic traits, such as production of the protective compound melanin. In C. neoformans, the pigment associates with key cellular constituents that are essential for melanin deposition within the cell wall. Consequently, melanization is modulated by changes in cell-wall composition or ultrastructure. However, whether similar factors influence melanization in C. gattii is unknown. Herein, we used transmission EM, biochemical assays, and solid-state NMR spectroscopy of representative isolates and "leaky melanin" mutant strains from each species complex to examine the compositional and structural factors governing cell-wall pigment deposition in C. neoformans and C. gattii. The principal findings were the following. 1) C. gattii R265 had an exceptionally high chitosan content compared with C. neoformans H99; a rich chitosan composition promoted homogeneous melanin distribution throughout the cell wall but did not increase the propensity of pigment deposition. 2) Strains from both species manifesting the leaky melanin phenotype had reduced chitosan content, which was compensated for by the production of lipids and other nonpolysaccharide constituents that depended on the species or mutation. 3) Changes in the relative rigidity of cell-wall chitin were associated with aberrant pigment retention, implicating cell-wall flexibility as an independent variable in cryptococcal melanin assembly. Overall, our results indicate that cell-wall composition and molecular architecture are critical factors for the anchoring and arrangement of melanin pigments in both C. neoformans and C. gattii species complexes.
Molecular Structure, cell wall, polysaccharides, virulence factor, opportunistic pathogen, nuclear magnetic resonance (NMR), fungi, Cryptococcus, solid-state NMR, melanin
Structure type: structural motif or average structure
Location inside paper: Fig. 6, chitosan
Trivial name: chitosan
Compound class: O-polysaccharide, cell wall polysaccharide, glucan, polysaccharide
Contained glycoepitopes: IEDB_135813,IEDB_137340,IEDB_141807,IEDB_151531,IEDB_153212,IEDB_241099,IEDB_423114,IEDB_423150,SB_74,SB_85
Methods: NMR-2D, acid hydrolysis, extraction, isotopic labeling, cell growth, derivatization, TEM, light microscopy, 13C CPMAS NMR, 13C-13C DARR NMR, 13C DPMAS NMR
Related record ID(s): 41553, 44877, 44886, 46311, 46570, 46683, 48760, 48774, 49133, 49502, 49512, 49524, 49653, 50016, 50301, 50303, 50304, 50307, 50308, 50310, 50312, 50314, 50315, 50317, 50319, 50320
NCBI Taxonomy refs (TaxIDs): 235443,
5207,
294750,
37769Reference(s) to other database(s): GTC:G97099AY
Show glycosyltransferases
There is only one chemically distinct structure:
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Chrissian C, Camacho E, Fu MS, Prados-Rosales R, Chatterjee S, Cordero RJB, Lodge JK, Casadevall A, Stark RE
Melanin deposition in two Cryptococcus species depends on cell-wall composition and flexibility
Journal of Biological Chemistry 295(7) (2020)
1815-1828
Cryptococcus neoformans H99
(later renamed to: Cryptococcus neoformans var. grubii H99)
(NCBI TaxID 235443,
species name lookup)
Cryptococcus neoformans ST211A
(Ancestor NCBI TaxID 5207,
species name lookup)
Cryptococcus gattii R265
(later renamed to: Cryptococcus gattii VGII R265)
(NCBI TaxID 294750,
species name lookup)
Cryptococcus gattii Cg53
(later renamed to: Cryptococcus gattii VGI Cg53)
(Ancestor NCBI TaxID 37769,
species name lookup)
Taxonomic group: fungi / Basidiomycota
(Phylum: Basidiomycota)
Organ / tissue: cell wallAssociated disease: infection due to Cryptococcus neoformans [ICD11:
XN3EH ];
infection due to Cryptococcus gattii [ICD11:
XN0LE ]
NCBI PubMed ID: 31896575Publication DOI: 10.1074/jbc.RA119.011949Journal NLM ID: 2985121RPublisher: Baltimore, MD: American Society for Biochemistry and Molecular Biology
Correspondence: rstark
ccny.cuny.edu
Institutions: Department of Preventive Medicine and Public Health and Microbiology, Autonoma University of Madrid, Madrid, Spain, Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, USA, Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, Johns Hopkins University, Baltimore, USA, Ph.D. Program in Biochemistry, The Graduate Center of the City University of New York, New York, NY, USA, Department of Chemistry and Biochemistry, City College of New York and CUNY Institute for Macromolecular Assemblies, New York, USA, Department of Microbiology and Immunology, Albert Einstein College of Medicine, Yeshiva University, Bronx, USA
Cryptococcus neoformans and Cryptococcus gattii are two species complexes in the large fungal genus Cryptococcus and are responsible for potentially lethal disseminated infections. These two complexes share several phenotypic traits, such as production of the protective compound melanin. In C. neoformans, the pigment associates with key cellular constituents that are essential for melanin deposition within the cell wall. Consequently, melanization is modulated by changes in cell-wall composition or ultrastructure. However, whether similar factors influence melanization in C. gattii is unknown. Herein, we used transmission EM, biochemical assays, and solid-state NMR spectroscopy of representative isolates and "leaky melanin" mutant strains from each species complex to examine the compositional and structural factors governing cell-wall pigment deposition in C. neoformans and C. gattii. The principal findings were the following. 1) C. gattii R265 had an exceptionally high chitosan content compared with C. neoformans H99; a rich chitosan composition promoted homogeneous melanin distribution throughout the cell wall but did not increase the propensity of pigment deposition. 2) Strains from both species manifesting the leaky melanin phenotype had reduced chitosan content, which was compensated for by the production of lipids and other nonpolysaccharide constituents that depended on the species or mutation. 3) Changes in the relative rigidity of cell-wall chitin were associated with aberrant pigment retention, implicating cell-wall flexibility as an independent variable in cryptococcal melanin assembly. Overall, our results indicate that cell-wall composition and molecular architecture are critical factors for the anchoring and arrangement of melanin pigments in both C. neoformans and C. gattii species complexes.
Molecular Structure, cell wall, polysaccharides, virulence factor, opportunistic pathogen, nuclear magnetic resonance (NMR), fungi, Cryptococcus, solid-state NMR, melanin
Structure type: homopolymer
Location inside paper: Fig. 6, chitin
Trivial name: chitin
Compound class: O-polysaccharide, cell wall polysaccharide, glucan, polysaccharide, chitin
Contained glycoepitopes: IEDB_135813,IEDB_137340,IEDB_141807,IEDB_151531,IEDB_153212,IEDB_241099,IEDB_423114,IEDB_423150,SB_74,SB_85
Methods: NMR-2D, acid hydrolysis, extraction, isotopic labeling, cell growth, derivatization, TEM, light microscopy, 13C CPMAS NMR, 13C-13C DARR NMR, 13C DPMAS NMR
Related record ID(s): 40760, 40800, 41831, 49862, 50302, 50305, 50306, 50309, 50311, 50313, 50316, 50318, 111874, 121703, 131817, 139821, 143656, 147987, 149876
NCBI Taxonomy refs (TaxIDs): 235443,
5207,
294750,
37769Reference(s) to other database(s): GTC:G97099AY, CCSD:
46067, CBank-STR:5851, GenDB:KF905651
Show glycosyltransferases
There is only one chemically distinct structure:
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