Alterations of the gut microbiome in HIV infection highlight human anelloviruses as potential predictors of immune recovery.

IF 13.8 1区 生物学 Q1 MICROBIOLOGY Microbiome Pub Date : 2024-10-17 DOI:10.1186/s40168-024-01925-7
Celia Boukadida, Amy Peralta-Prado, Monserrat Chávez-Torres, Karla Romero-Mora, Alma Rincon-Rubio, Santiago Ávila-Ríos, Daniela Garrido-Rodríguez, Gustavo Reyes-Terán, Sandra Pinto-Cardoso
{"title":"Alterations of the gut microbiome in HIV infection highlight human anelloviruses as potential predictors of immune recovery.","authors":"Celia Boukadida, Amy Peralta-Prado, Monserrat Chávez-Torres, Karla Romero-Mora, Alma Rincon-Rubio, Santiago Ávila-Ríos, Daniela Garrido-Rodríguez, Gustavo Reyes-Terán, Sandra Pinto-Cardoso","doi":"10.1186/s40168-024-01925-7","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>HIV-1 infection is characterized by a massive depletion of mucosal CD4 T cells that triggers a cascade of events ultimately linking gut microbial dysbiosis to HIV-1 disease progression and pathogenesis. The association between HIV infection and the enteric virome composition is less characterized, although viruses are an essential component of the gut ecosystem. Here, we performed a cross-sectional analysis of the fecal viral (eukaryotic viruses and bacteriophages) and bacterial microbiome in people with HIV (PWH) and in HIV-negative individuals. To gain further insight into the association between the gut microbiome composition, HIV-associated immunodeficiency, and immune recovery, we carried out a longitudinal study including 14 PWH who initiated antiretroviral therapy (ART) and were followed for 24 months with samplings performed at baseline (before ART) and at 2, 6, 12, and 24 months post-ART initiation.</p><p><strong>Results: </strong>Our data revealed a striking expansion in the abundance and prevalence of several human virus genomic sequences (Anelloviridae, Adenoviridae, and Papillomaviridae) in stool samples of PWH with severe immunodeficiency (CD4 < 200). We also noted a decreased abundance of sequences belonging to two plant viruses from the Tobamovirus genus, a reduction in bacterial alpha diversity, and a decrease in Inoviridae bacteriophage sequences. Short-term ART (24 months) was linked to a significant decrease in human Anelloviridae sequences. Remarkably, the detection of Anellovirus sequences at baseline independently predicted poor immune recovery, as did low CD4 T cell counts. The bacterial and bacteriophage populations were unique to each PWH with individualized trajectories; we found no discernable pattern of clustering after 24 months on ART.</p><p><strong>Conclusion: </strong>Advanced HIV-1 infection was associated with marked alterations in the virome composition, in particular a remarkable expansion of human anelloviruses, with a gradual restoration after ART initiation. In addition to CD4 T cell counts, anellovirus sequence detection might be useful to predict and monitor immune recovery. This study confirms data on the bacteriome and expands our knowledge on the viral component of the gut microbiome in HIV-1 infection. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":null,"pages":null},"PeriodicalIF":13.8000,"publicationDate":"2024-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11483978/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Microbiome","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1186/s40168-024-01925-7","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Background: HIV-1 infection is characterized by a massive depletion of mucosal CD4 T cells that triggers a cascade of events ultimately linking gut microbial dysbiosis to HIV-1 disease progression and pathogenesis. The association between HIV infection and the enteric virome composition is less characterized, although viruses are an essential component of the gut ecosystem. Here, we performed a cross-sectional analysis of the fecal viral (eukaryotic viruses and bacteriophages) and bacterial microbiome in people with HIV (PWH) and in HIV-negative individuals. To gain further insight into the association between the gut microbiome composition, HIV-associated immunodeficiency, and immune recovery, we carried out a longitudinal study including 14 PWH who initiated antiretroviral therapy (ART) and were followed for 24 months with samplings performed at baseline (before ART) and at 2, 6, 12, and 24 months post-ART initiation.

Results: Our data revealed a striking expansion in the abundance and prevalence of several human virus genomic sequences (Anelloviridae, Adenoviridae, and Papillomaviridae) in stool samples of PWH with severe immunodeficiency (CD4 < 200). We also noted a decreased abundance of sequences belonging to two plant viruses from the Tobamovirus genus, a reduction in bacterial alpha diversity, and a decrease in Inoviridae bacteriophage sequences. Short-term ART (24 months) was linked to a significant decrease in human Anelloviridae sequences. Remarkably, the detection of Anellovirus sequences at baseline independently predicted poor immune recovery, as did low CD4 T cell counts. The bacterial and bacteriophage populations were unique to each PWH with individualized trajectories; we found no discernable pattern of clustering after 24 months on ART.

Conclusion: Advanced HIV-1 infection was associated with marked alterations in the virome composition, in particular a remarkable expansion of human anelloviruses, with a gradual restoration after ART initiation. In addition to CD4 T cell counts, anellovirus sequence detection might be useful to predict and monitor immune recovery. This study confirms data on the bacteriome and expands our knowledge on the viral component of the gut microbiome in HIV-1 infection. Video Abstract.

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
艾滋病毒感染中肠道微生物组的改变凸显了人类无肠道病毒作为免疫恢复潜在预测因子的作用。
背景:HIV-1 感染的特点是粘膜 CD4 T 细胞大量耗竭,从而引发一系列事件,最终将肠道微生物菌群失调与 HIV-1 疾病进展和发病机制联系起来。尽管病毒是肠道生态系统的重要组成部分,但 HIV 感染与肠道病毒组组成之间的关系却不太明确。在此,我们对 HIV 感染者(PWH)和 HIV 阴性个体的粪便病毒(真核病毒和噬菌体)和细菌微生物组进行了横断面分析。为了进一步了解肠道微生物组的组成、艾滋病相关免疫缺陷和免疫恢复之间的关系,我们开展了一项纵向研究,其中包括 14 名开始接受抗逆转录病毒疗法(ART)的艾滋病病毒感染者,并对他们进行了长达 24 个月的随访,在基线期(开始接受抗逆转录病毒疗法之前)和开始接受抗逆转录病毒疗法后的 2、6、12 和 24 个月进行采样:我们的数据显示,在患有严重免疫缺陷(CD4 结语)的 PWH 粪便样本中,几种人类病毒基因组序列(Anelloviridae、Adenoviridae 和 Papillomaviridae)的丰度和流行率显著增加:晚期 HIV-1 感染与病毒组组成的明显改变有关,尤其是人类无病毒科病毒的显著扩增,在开始接受抗逆转录病毒疗法后病毒组组成逐渐恢复。除了 CD4 T 细胞计数外,鼻疽病毒序列检测可能有助于预测和监测免疫恢复情况。这项研究证实了细菌组的数据,并扩展了我们对 HIV-1 感染者肠道微生物组病毒成分的认识。视频摘要。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 去求助
来源期刊
Microbiome
Microbiome MICROBIOLOGY-
CiteScore
21.90
自引率
2.60%
发文量
198
审稿时长
4 weeks
期刊介绍: Microbiome is a journal that focuses on studies of microbiomes in humans, animals, plants, and the environment. It covers both natural and manipulated microbiomes, such as those in agriculture. The journal is interested in research that uses meta-omics approaches or novel bioinformatics tools and emphasizes the community/host interaction and structure-function relationship within the microbiome. Studies that go beyond descriptive omics surveys and include experimental or theoretical approaches will be considered for publication. The journal also encourages research that establishes cause and effect relationships and supports proposed microbiome functions. However, studies of individual microbial isolates/species without exploring their impact on the host or the complex microbiome structures and functions will not be considered for publication. Microbiome is indexed in BIOSIS, Current Contents, DOAJ, Embase, MEDLINE, PubMed, PubMed Central, and Science Citations Index Expanded.
期刊最新文献
Intestinal commensal bacteria promote Bactrocera dorsalis larval development through the vitamin B6 synthesis pathway. MAGqual: a stand-alone pipeline to assess the quality of metagenome-assembled genomes. Nepali oral microbiomes reflect a gradient of lifestyles from traditional to industrialized. The gut microbiome in patients with Cushing's disease affects depression- and anxiety-like behavior in mice. Quality traits drive the enrichment of Massilia in the rhizosphere to improve soybean oil content.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 联系我们:info@booksci.cn
Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。
Copyright © 2023 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1