Diversity and Complexity of the Large Surface Protein Family in the Compacted Genomes of Multiple <italic toggle="yes">Pneumocystis</italic> Species
ABSTRACT Pneumocystis, a major opportunistic pathogen in patients with a broad range of immunodeficiencies, contains abundant surface proteins encoded by a multicopy gene family, termed the major surface glycoprotein (Msg) gene superfamily. This superfamily has been identified in all Pneumocystis sp...
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American Society for Microbiology
2020
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oai:doaj.org-article:506cf3cdb75d42c089e62b4f90d2fba52021-11-15T15:57:02ZDiversity and Complexity of the Large Surface Protein Family in the Compacted Genomes of Multiple <italic toggle="yes">Pneumocystis</italic> Species10.1128/mBio.02878-192150-7511https://doaj.org/article/506cf3cdb75d42c089e62b4f90d2fba52020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02878-19https://doaj.org/toc/2150-7511ABSTRACT Pneumocystis, a major opportunistic pathogen in patients with a broad range of immunodeficiencies, contains abundant surface proteins encoded by a multicopy gene family, termed the major surface glycoprotein (Msg) gene superfamily. This superfamily has been identified in all Pneumocystis species characterized to date, highlighting its important role in Pneumocystis biology. In this report, through a comprehensive and in-depth characterization of 459 msg genes from 7 Pneumocystis species, we demonstrate, for the first time, the phylogeny and evolution of conserved domains in Msg proteins and provide a detailed description of the classification, unique characteristics, and phylogenetic relatedness of five Msg families. We further describe, for the first time, the relative expression levels of individual msg families in two rodent Pneumocystis species, the substantial variability of the msg repertoires in P. carinii from laboratory and wild rats, and the distinct features of the expression site for the classic msg genes in Pneumocystis from 8 mammalian host species. Our analysis suggests multiple functions for this superfamily rather than just conferring antigenic variation to allow immune evasion as previously believed. This study provides a rich source of information that lays the foundation for the continued experimental exploration of the functions of the Msg superfamily in Pneumocystis biology. IMPORTANCE Pneumocystis continues to be a major cause of disease in humans with immunodeficiency, especially those with HIV/AIDS and organ transplants, and is being seen with increasing frequency worldwide in patients treated with immunodepleting monoclonal antibodies. Annual health care associated with Pneumocystis pneumonia costs ∼$475 million dollars in the United States alone. In addition to causing overt disease in immunodeficient individuals, Pneumocystis can cause subclinical infection or colonization in healthy individuals, which may play an important role in species preservation and disease transmission. Our work sheds new light on the diversity and complexity of the msg superfamily and strongly suggests that the versatility of this superfamily reflects multiple functions, including antigenic variation to allow immune evasion and optimal adaptation to host environmental conditions to promote efficient infection and transmission. These findings are essential to consider in developing new diagnostic and therapeutic strategies.Liang MaZehua ChenDa Wei HuangOusmane H. CisséJamie L. RothenburgerAlice LatinneLisa BishopRobert BlairJason M. BrenchleyMagali ChabéXilong DengVanessa HirschRebekah KeeslerGeetha KuttyYueqin LiuDaniel MargolisSerge MorandBapi PaharLi PengKoen K. A. Van RompayXiaohong SongJun SongAntti SukuraSabrina ThaparHonghui WangChristiane Weissenbacher-LangJie XuChao-Hung LeeClaire JardineRichard A. LempickiMelanie T. CushionChristina A. CuomoJoseph A. KovacsAmerican Society for Microbiologyarticleclassificationconserved domainsmajor surface glycoproteinphylogenetic analysisPneumocystisMicrobiologyQR1-502ENmBio, Vol 11, Iss 2 (2020) |
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DOAJ |
| collection |
DOAJ |
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EN |
| topic |
classification conserved domains major surface glycoprotein phylogenetic analysis Pneumocystis Microbiology QR1-502 |
| spellingShingle |
classification conserved domains major surface glycoprotein phylogenetic analysis Pneumocystis Microbiology QR1-502 Liang Ma Zehua Chen Da Wei Huang Ousmane H. Cissé Jamie L. Rothenburger Alice Latinne Lisa Bishop Robert Blair Jason M. Brenchley Magali Chabé Xilong Deng Vanessa Hirsch Rebekah Keesler Geetha Kutty Yueqin Liu Daniel Margolis Serge Morand Bapi Pahar Li Peng Koen K. A. Van Rompay Xiaohong Song Jun Song Antti Sukura Sabrina Thapar Honghui Wang Christiane Weissenbacher-Lang Jie Xu Chao-Hung Lee Claire Jardine Richard A. Lempicki Melanie T. Cushion Christina A. Cuomo Joseph A. Kovacs Diversity and Complexity of the Large Surface Protein Family in the Compacted Genomes of Multiple <italic toggle="yes">Pneumocystis</italic> Species |
| description |
ABSTRACT Pneumocystis, a major opportunistic pathogen in patients with a broad range of immunodeficiencies, contains abundant surface proteins encoded by a multicopy gene family, termed the major surface glycoprotein (Msg) gene superfamily. This superfamily has been identified in all Pneumocystis species characterized to date, highlighting its important role in Pneumocystis biology. In this report, through a comprehensive and in-depth characterization of 459 msg genes from 7 Pneumocystis species, we demonstrate, for the first time, the phylogeny and evolution of conserved domains in Msg proteins and provide a detailed description of the classification, unique characteristics, and phylogenetic relatedness of five Msg families. We further describe, for the first time, the relative expression levels of individual msg families in two rodent Pneumocystis species, the substantial variability of the msg repertoires in P. carinii from laboratory and wild rats, and the distinct features of the expression site for the classic msg genes in Pneumocystis from 8 mammalian host species. Our analysis suggests multiple functions for this superfamily rather than just conferring antigenic variation to allow immune evasion as previously believed. This study provides a rich source of information that lays the foundation for the continued experimental exploration of the functions of the Msg superfamily in Pneumocystis biology. IMPORTANCE Pneumocystis continues to be a major cause of disease in humans with immunodeficiency, especially those with HIV/AIDS and organ transplants, and is being seen with increasing frequency worldwide in patients treated with immunodepleting monoclonal antibodies. Annual health care associated with Pneumocystis pneumonia costs ∼$475 million dollars in the United States alone. In addition to causing overt disease in immunodeficient individuals, Pneumocystis can cause subclinical infection or colonization in healthy individuals, which may play an important role in species preservation and disease transmission. Our work sheds new light on the diversity and complexity of the msg superfamily and strongly suggests that the versatility of this superfamily reflects multiple functions, including antigenic variation to allow immune evasion and optimal adaptation to host environmental conditions to promote efficient infection and transmission. These findings are essential to consider in developing new diagnostic and therapeutic strategies. |
| format |
article |
| author |
Liang Ma Zehua Chen Da Wei Huang Ousmane H. Cissé Jamie L. Rothenburger Alice Latinne Lisa Bishop Robert Blair Jason M. Brenchley Magali Chabé Xilong Deng Vanessa Hirsch Rebekah Keesler Geetha Kutty Yueqin Liu Daniel Margolis Serge Morand Bapi Pahar Li Peng Koen K. A. Van Rompay Xiaohong Song Jun Song Antti Sukura Sabrina Thapar Honghui Wang Christiane Weissenbacher-Lang Jie Xu Chao-Hung Lee Claire Jardine Richard A. Lempicki Melanie T. Cushion Christina A. Cuomo Joseph A. Kovacs |
| author_facet |
Liang Ma Zehua Chen Da Wei Huang Ousmane H. Cissé Jamie L. Rothenburger Alice Latinne Lisa Bishop Robert Blair Jason M. Brenchley Magali Chabé Xilong Deng Vanessa Hirsch Rebekah Keesler Geetha Kutty Yueqin Liu Daniel Margolis Serge Morand Bapi Pahar Li Peng Koen K. A. Van Rompay Xiaohong Song Jun Song Antti Sukura Sabrina Thapar Honghui Wang Christiane Weissenbacher-Lang Jie Xu Chao-Hung Lee Claire Jardine Richard A. Lempicki Melanie T. Cushion Christina A. Cuomo Joseph A. Kovacs |
| author_sort |
Liang Ma |
| title |
Diversity and Complexity of the Large Surface Protein Family in the Compacted Genomes of Multiple <italic toggle="yes">Pneumocystis</italic> Species |
| title_short |
Diversity and Complexity of the Large Surface Protein Family in the Compacted Genomes of Multiple <italic toggle="yes">Pneumocystis</italic> Species |
| title_full |
Diversity and Complexity of the Large Surface Protein Family in the Compacted Genomes of Multiple <italic toggle="yes">Pneumocystis</italic> Species |
| title_fullStr |
Diversity and Complexity of the Large Surface Protein Family in the Compacted Genomes of Multiple <italic toggle="yes">Pneumocystis</italic> Species |
| title_full_unstemmed |
Diversity and Complexity of the Large Surface Protein Family in the Compacted Genomes of Multiple <italic toggle="yes">Pneumocystis</italic> Species |
| title_sort |
diversity and complexity of the large surface protein family in the compacted genomes of multiple <italic toggle="yes">pneumocystis</italic> species |
| publisher |
American Society for Microbiology |
| publishDate |
2020 |
| url |
https://doaj.org/article/506cf3cdb75d42c089e62b4f90d2fba5 |
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