Glycan cross-feeding supports mutualism between Fusobacterium and the vaginal microbiota

被引:36
作者
Agarwal, Kavita [1 ,2 ,8 ]
Robinson, Lloyd S. [1 ,2 ]
Aggarwal, Somya [1 ,2 ]
Foster, Lynne R. [1 ,2 ]
Hernandez-Leyva, Ariel [2 ,3 ]
Lin, Hueylie [1 ,2 ]
Tortelli, Brett A. [2 ,4 ]
O'Brien, Valerie P. [1 ,2 ]
Miller, Liza [1 ,2 ]
Kau, Andrew L. [2 ,3 ]
Reno, Hilary [5 ]
Gilbert, Nicole M. [2 ,6 ,7 ]
Lewis, Warren G. [1 ,2 ,8 ]
Lewis, Amanda L. [1 ,2 ,6 ,8 ]
机构
[1] Washington Univ, Sch Med, Dept Mol Microbiol, St Louis, MO 63110 USA
[2] Washington Univ, Sch Med, Ctr Womens Infect Dis Res, St Louis, MO 63110 USA
[3] Washington Univ, Sch Med, Dept Med, Div Allergy & Immunol, St Louis, MO 63110 USA
[4] Washington Univ, Sch Med, Dept Genet, St Louis, MO 63110 USA
[5] Washington Univ, Dept Med, Div Infect Dis, Sch Med, St Louis, MO USA
[6] Washington Univ, Sch Med, Dept Obstet & Gynecol, St Louis, MO 63110 USA
[7] Washington Univ, Sch Med, Ctr Reprod Hlth Sci, St Louis, MO USA
[8] Univ Calif San Diego, Dept Obstet Gynecol & Reprod Sci, Glycobiol Res & Training Ctr, La Jolla, CA 92093 USA
关键词
N-ACETYLNEURAMINATE LYASE; SIALATE O-ACETYLESTERASE; BACTERIAL VAGINOSIS; NEURAMINIDASE ACTIVITY; GARDNERELLA-VAGINALIS; CRYSTAL-STRUCTURES; ESCHERICHIA-COLI; EPITHELIAL-CELLS; GENE-EXPRESSION; SIALIDASE;
D O I
10.1371/journal.pbio.3000788
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Women with bacterial vaginosis (BV), an imbalance of the vaginal microbiome, are more likely to be colonized by potential pathogens such asFusobacterium nucleatum, a bacterium linked with intrauterine infection and preterm birth. However, the conditions and mechanisms supporting pathogen colonization during vaginal dysbiosis remain obscure. We demonstrate that sialidase activity, a diagnostic feature of BV, promotedF.nucleatumforaging and growth on mammalian sialoglycans, a nutrient resource that was otherwise inaccessible because of the lack of endogenousF.nucleatumsialidase. In mice with sialidase-producing vaginal microbiotas, mutantF.nucleatumunable to consume sialic acids was impaired in vaginal colonization. These experiments in mice also led to the discovery thatF.nucleatummay also "give back" to the community by reinforcing sialidase activity, a biochemical feature of human dysbiosis. Using human vaginal bacterial communities, we show thatF.nucleatumsupported robust outgrowth ofGardnerella vaginalis, a major sialidase producer and one of the most abundant organisms in BV. These results illustrate that mutually beneficial relationships between vaginal bacteria support pathogen colonization and may help maintain features of dysbiosis. These findings challenge the simplistic dogma that the mere absence of "healthy" lactobacilli is the sole mechanism that creates a permissive environment for pathogens during vaginal dysbiosis. Given the ubiquity ofF.nucleatumin the human mouth, these studies also suggest a possible mechanism underlying links between vaginal dysbiosis and oral sex.
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页数:36
相关论文
共 95 条
[1]   Prevalence of bacterial vaginosis - 2001-2004 National Health and Nutrition Examination Survey data [J].
Allsworth, Jenifer E. ;
Peipert, Jeffrey F. .
OBSTETRICS AND GYNECOLOGY, 2007, 109 (01) :114-120
[2]   Gapped BLAST and PSI-BLAST: a new generation of protein database search programs [J].
Altschul, SF ;
Madden, TL ;
Schaffer, AA ;
Zhang, JH ;
Zhang, Z ;
Miller, W ;
Lipman, DJ .
NUCLEIC ACIDS RESEARCH, 1997, 25 (17) :3389-3402
[3]   Identification, quantification and subtyping of Gardnerella vaginalis in noncultured clinical vaginal samples by quantitative PCR [J].
Balashov, Sergey V. ;
Mordechai, Eli ;
Adelson, Martin E. ;
Gygax, Scott E. .
JOURNAL OF MEDICAL MICROBIOLOGY, 2014, 63 :162-175
[4]  
Belzer C, 2017, MBIO, V8, DOI [10.1128/mBio.00770-17, 10.1128/mbio.00770-17]
[5]   Gut Microbiota, Inflammation, and Colorectal Cancer [J].
Brennan, Caitlin A. ;
Garrett, Wendy S. .
ANNUAL REVIEW OF MICROBIOLOGY, VOL 70, 2016, 70 :395-411
[6]   SIALIDASES (NEURAMINIDASES) IN BACTERIAL VAGINOSIS AND BACTERIAL VAGINOSIS-ASSOCIATED MICROFLORA [J].
BRISELDEN, AM ;
MONCLA, BJ ;
STEVENS, CE ;
HILLIER, SL .
JOURNAL OF CLINICAL MICROBIOLOGY, 1992, 30 (03) :663-666
[7]   Bacterial Vaginosis Assessed by Gram Stain and Diminished Colonization Resistance to Incident Gonococcal, Chlamydial, and Trichomonal Genital Infection [J].
Brotman, Rebecca M. ;
Klebanoff, Mark A. ;
Nansel, Tonja R. ;
Yu, Kai F. ;
Andrews, William W. ;
Zhang, Jun ;
Schwebke, Jane R. .
JOURNAL OF INFECTIOUS DISEASES, 2010, 202 (12) :1907-1915
[8]   Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer [J].
Bullman, Susan ;
Pedamallu, Chandra S. ;
Sicinska, Ewa ;
Claney, Thomas E. ;
Zhang, Xiaoyang ;
Cai, Diana ;
Neuberg, Donna ;
Huang, Katherine ;
Guevara, Fatima ;
Nelson, Timothy ;
Chipashvili, Otari ;
Hagan, Timothy ;
Walker, Mark ;
Ramachandran, Aruna ;
Diosdado, Begona ;
Serna, Garazi ;
Mulet, Nuria ;
Landolfi, Stefania ;
Ramon y Cajal, Santiago ;
Fasani, Roberta ;
Aguirre, Andrew J. ;
Ng, Kimmie ;
Elez, Elena ;
Ogino, Shuji ;
Tabernero, Josep ;
Fuchs, Charles S. ;
Hahn, William C. ;
Nuciforo, Paolo ;
Meyerson, Matthew .
SCIENCE, 2017, 358 (6369) :1443-+
[9]   Crystal structure of N-acetylmannosamine kinase from Fusobacterium nucleatum [J].
Caing-Carlsson, Rhawnie ;
Goyal, Parveen ;
Sharma, Amit ;
Ghosh, Swagatha ;
Setty, Thanuja Gangi ;
North, Rachel A. ;
Friemann, Rosmarie ;
Ramaswamy, S. .
ACTA CRYSTALLOGRAPHICA SECTION F-STRUCTURAL BIOLOGY COMMUNICATIONS, 2017, 73 :356-362
[10]  
Callahan BJ, 2016, NAT METHODS, V13, P581, DOI [10.1038/NMETH.3869, 10.1038/nmeth.3869]