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Shifts in microbial diversity, composition, and functionality in the gut and genital microbiome during a natural SIV infection in vervet monkeys
Microbiome ( IF 15.5 ) Pub Date : 2020-11-06 , DOI: 10.1186/s40168-020-00928-4
Anna J. Jasinska , Tien S. Dong , Venu Lagishetty , William Katzka , Jonathan P. Jacobs , Christopher A. Schmitt , Jennifer Danzy Cramer , Dongzhu Ma , Willem G. Coetzer , J. Paul Grobler , Trudy R. Turner , Nelson Freimer , Ivona Pandrea , Cristian Apetrei

The microbiota plays an important role in HIV pathogenesis in humans. Microbiota can impact health through several pathways such as increasing inflammation in the gut, metabolites of bacterial origin, and microbial translocation from the gut to the periphery which contributes to systemic chronic inflammation and immune activation and the development of AIDS. Unlike HIV-infected humans, SIV-infected vervet monkeys do not experience gut dysfunction, microbial translocation, and chronic immune activation and do not progress to immunodeficiency. Here, we provide the first reported characterization of the microbial ecosystems of the gut and genital tract in a natural nonprogressing host of SIV, wild vervet monkeys from South Africa. We characterized fecal, rectal, vaginal, and penile microbiomes in vervets from populations heavily infected with SIV from diverse locations across South Africa. Geographic site, age, and sex affected the vervet microbiome across different body sites. Fecal and vaginal microbiome showed marked stratification with three enterotypes in fecal samples and two vagitypes, which were predicted functionally distinct within each body site. External bioclimatic factors, biome type, and environmental temperature influenced microbiomes locally associated with vaginal and rectal mucosa. Several fecal microbial taxa were linked to plasma levels of immune molecules, for example, MIG was positively correlated with Lactobacillus and Escherichia/Shigella and Helicobacter, and IL-10 was negatively associated with Erysipelotrichaceae, Anaerostipes, Prevotella, and Anaerovibrio, and positively correlated with Bacteroidetes and Succinivibrio. During the chronic phase of infection, we observed a significant increase in gut microbial diversity, alterations in community composition (including a decrease in Proteobacteria/Succinivibrio in the gut) and functionality (including a decrease in genes involved in bacterial invasion of epithelial cells in the gut), and partial reversibility of acute infection-related shifts in microbial abundance observed in the fecal microbiome. As part of our study, we also developed an accurate predictor of SIV infection using fecal samples. The vervets infected with SIV and humans infected with HIV differ in microbial responses to infection. These responses to SIV infection may aid in preventing microbial translocation and subsequent disease progression in vervets, and may represent host microbiome adaptations to the virus.

中文翻译:

黑长尾猴自然SIV感染过程中肠道和生殖器微生物组中微生物多样性,组成和功能的变化

微生物群在人类HIV发病机理中起重要作用。微生物群可以通过几种途径影响健康,例如增加肠道中的炎症,细菌起源的代谢产物以及微生物从肠道到周围的移位,从而导致全身性慢性炎症和免疫活化以及艾滋病的发展。与感染HIV的人类不同,感染SIV的黑长尾猴不会出现肠道功能障碍,微生物易位和慢性免疫激活,并且不会发展为免疫缺陷。在这里,我们提供了首次报道的天然无进展宿主SIV(来自南非的野生黑长尾猴)中肠道和生殖道微生物生态系统的特征。我们对粪便,直肠,阴道,来自南非各地的严重感染了SIV的人群的黑醋栗和阴茎微生物群系。地理位置,年龄和性别影响了不同身体部位的vervet微生物组。粪便和阴道微生物组显示出明显的分层,粪便样品中有三种肠型和两种阴道型,这被预测在每个身体部位的功能不同。外部生物气候因素,生物群落类型和环境温度影响与阴道和直肠粘膜局部相关的微生物群落。几种粪便微生物分类群与血浆中的免疫分子水平相关,例如,MIG与乳杆菌,大肠埃希氏菌/志贺氏菌和幽门螺杆菌呈正相关,而IL-10与丹参,厌氧杆菌,普氏杆菌和Anaerovibrio呈负相关,与拟杆菌和琥珀弧菌呈正相关。在感染的慢性期,我们观察到肠道微生物多样性显着增加,群落组成发生改变(包括肠道内Proteobacteria / Succinivibrio减少)和功能性(包括参与细菌侵袭上皮细胞的基因减少)肠道微生物),以及在粪便微生物组中观察到的与急性感染相关的微生物丰度变化的部分可逆性。作为研究的一部分,我们还使用粪便样本开发了SIV感染的准确预测指标。被SIV感染的黑长春和被HIV感染的人在微生物对感染的反应方面有所不同。这些对SIV感染的反应可能有助于防止微生物迁移以及黑醋栗中随后的疾病进展,
更新日期:2020-11-06
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