<italic toggle="yes">O</italic>-Mannosylation in <named-content content-type="genus-species">Candida albicans</named-content> Enables Development of Interkingdom Biofilm Communities
ABSTRACT Candida albicans is a fungus that colonizes oral cavity surfaces, the gut, and the genital tract. Streptococcus gordonii is a ubiquitous oral bacterium that has been shown to form biofilm communities with C. albicans. Formation of dual-species S. gordonii-C. albicans biofilm communities inv...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2014-05-01
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| Series: | mBio |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.00911-14 |
| _version_ | 1818987277314949120 |
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| author | Lindsay C. Dutton Angela H. Nobbs Katy Jepson Mark A. Jepson M. Margaret Vickerman Sami Aqeel Alawfi Carol A. Munro Richard J. Lamont Howard F. Jenkinson |
| author_facet | Lindsay C. Dutton Angela H. Nobbs Katy Jepson Mark A. Jepson M. Margaret Vickerman Sami Aqeel Alawfi Carol A. Munro Richard J. Lamont Howard F. Jenkinson |
| author_sort | Lindsay C. Dutton |
| collection | DOAJ |
| description | ABSTRACT Candida albicans is a fungus that colonizes oral cavity surfaces, the gut, and the genital tract. Streptococcus gordonii is a ubiquitous oral bacterium that has been shown to form biofilm communities with C. albicans. Formation of dual-species S. gordonii-C. albicans biofilm communities involves interaction of the S. gordonii SspB protein with the Als3 protein on the hyphal filament surface of C. albicans. Mannoproteins comprise a major component of the C. albicans cell wall, and in this study we sought to determine if mannosylation in cell wall biogenesis of C. albicans was necessary for hyphal adhesin functions associated with interkingdom biofilm development. A C. albicans mnt1Δ mnt2Δ mutant, with deleted α-1,2-mannosyltransferase genes and thus defective in O-mannosylation, was abrogated in biofilm formation under various growth conditions and produced hyphal filaments that were not recognized by S. gordonii. Cell wall proteomes of hypha-forming mnt1Δ mnt2Δ mutant cells showed growth medium-dependent alterations, compared to findings for the wild type, in a range of protein components, including Als1, Als3, Rbt1, Scw1, and Sap9. Hyphal filaments formed by mnt1Δ mnt2Δ mutant cells, unlike wild-type hyphae, did not interact with C. albicans Als3 or Hwp1 partner cell wall proteins or with S. gordonii SspB partner adhesin, suggesting defective functionality of adhesins on the mnt1Δ mnt2Δ mutant. These observations imply that early stage O-mannosylation is critical for activation of hyphal adhesin functions required for biofilm formation, recognition by bacteria such as S. gordonii, and microbial community development. IMPORTANCE In the human mouth, microorganisms form communities known as biofilms that adhere to the surfaces present. Candida albicans is a fungus that is often found within these biofilms. We have focused on the mechanisms by which C. albicans becomes incorporated into communities containing bacteria, such as Streptococcus. We find that impairment of early stage addition of mannose sugars to C. albicans hyphal filament proteins deleteriously affects their subsequent performance in mediating formation of polymicrobial biofilms. Our analyses provide new understanding of the way that microbial communities develop, and of potential means to control C. albicans infections. |
| first_indexed | 2024-12-20T19:04:08Z |
| format | Article |
| id | doaj.art-07c4261ac2b84ba6b459a69cc1ff14e4 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-20T19:04:08Z |
| publishDate | 2014-05-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-07c4261ac2b84ba6b459a69cc1ff14e42022-12-21T19:29:18ZengAmerican Society for MicrobiologymBio2150-75112014-05-015210.1128/mBio.00911-14<italic toggle="yes">O</italic>-Mannosylation in <named-content content-type="genus-species">Candida albicans</named-content> Enables Development of Interkingdom Biofilm CommunitiesLindsay C. Dutton0Angela H. Nobbs1Katy Jepson2Mark A. Jepson3M. Margaret Vickerman4Sami Aqeel Alawfi5Carol A. Munro6Richard J. Lamont7Howard F. Jenkinson8School of Oral and Dental Sciences, University of Bristol, Bristol, United KingdomSchool of Oral and Dental Sciences, University of Bristol, Bristol, United KingdomSchool of Biochemistry, University of Bristol, Bristol, United KingdomSchool of Biochemistry, University of Bristol, Bristol, United KingdomSchool of Dental Medicine, University at Buffalo, Buffalo, New York, USAInstitute of Medical Sciences, University of Aberdeen, Aberdeen, ScotlandInstitute of Medical Sciences, University of Aberdeen, Aberdeen, ScotlandSchool of Dentistry, University of Louisville, Louisville, Kentucky, USASchool of Oral and Dental Sciences, University of Bristol, Bristol, United KingdomABSTRACT Candida albicans is a fungus that colonizes oral cavity surfaces, the gut, and the genital tract. Streptococcus gordonii is a ubiquitous oral bacterium that has been shown to form biofilm communities with C. albicans. Formation of dual-species S. gordonii-C. albicans biofilm communities involves interaction of the S. gordonii SspB protein with the Als3 protein on the hyphal filament surface of C. albicans. Mannoproteins comprise a major component of the C. albicans cell wall, and in this study we sought to determine if mannosylation in cell wall biogenesis of C. albicans was necessary for hyphal adhesin functions associated with interkingdom biofilm development. A C. albicans mnt1Δ mnt2Δ mutant, with deleted α-1,2-mannosyltransferase genes and thus defective in O-mannosylation, was abrogated in biofilm formation under various growth conditions and produced hyphal filaments that were not recognized by S. gordonii. Cell wall proteomes of hypha-forming mnt1Δ mnt2Δ mutant cells showed growth medium-dependent alterations, compared to findings for the wild type, in a range of protein components, including Als1, Als3, Rbt1, Scw1, and Sap9. Hyphal filaments formed by mnt1Δ mnt2Δ mutant cells, unlike wild-type hyphae, did not interact with C. albicans Als3 or Hwp1 partner cell wall proteins or with S. gordonii SspB partner adhesin, suggesting defective functionality of adhesins on the mnt1Δ mnt2Δ mutant. These observations imply that early stage O-mannosylation is critical for activation of hyphal adhesin functions required for biofilm formation, recognition by bacteria such as S. gordonii, and microbial community development. IMPORTANCE In the human mouth, microorganisms form communities known as biofilms that adhere to the surfaces present. Candida albicans is a fungus that is often found within these biofilms. We have focused on the mechanisms by which C. albicans becomes incorporated into communities containing bacteria, such as Streptococcus. We find that impairment of early stage addition of mannose sugars to C. albicans hyphal filament proteins deleteriously affects their subsequent performance in mediating formation of polymicrobial biofilms. Our analyses provide new understanding of the way that microbial communities develop, and of potential means to control C. albicans infections.https://journals.asm.org/doi/10.1128/mBio.00911-14 |
| spellingShingle | Lindsay C. Dutton Angela H. Nobbs Katy Jepson Mark A. Jepson M. Margaret Vickerman Sami Aqeel Alawfi Carol A. Munro Richard J. Lamont Howard F. Jenkinson <italic toggle="yes">O</italic>-Mannosylation in <named-content content-type="genus-species">Candida albicans</named-content> Enables Development of Interkingdom Biofilm Communities mBio |
| title | <italic toggle="yes">O</italic>-Mannosylation in <named-content content-type="genus-species">Candida albicans</named-content> Enables Development of Interkingdom Biofilm Communities |
| title_full | <italic toggle="yes">O</italic>-Mannosylation in <named-content content-type="genus-species">Candida albicans</named-content> Enables Development of Interkingdom Biofilm Communities |
| title_fullStr | <italic toggle="yes">O</italic>-Mannosylation in <named-content content-type="genus-species">Candida albicans</named-content> Enables Development of Interkingdom Biofilm Communities |
| title_full_unstemmed | <italic toggle="yes">O</italic>-Mannosylation in <named-content content-type="genus-species">Candida albicans</named-content> Enables Development of Interkingdom Biofilm Communities |
| title_short | <italic toggle="yes">O</italic>-Mannosylation in <named-content content-type="genus-species">Candida albicans</named-content> Enables Development of Interkingdom Biofilm Communities |
| title_sort | italic toggle yes o italic mannosylation in named content content type genus species candida albicans named content enables development of interkingdom biofilm communities |
| url | https://journals.asm.org/doi/10.1128/mBio.00911-14 |
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