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Translocated microbiome composition determines immunological outcome in treated HIV infection.

ABSTRACT: The impact of the microbiome on HIV disease is widely acknowledged although the mechanisms downstream of fluctuations in microbial composition remain speculative. We detected rapid, dynamic changes in translocated microbial constituents during two years after cART initiation. An unbiased systems biology approach revealed two distinct pathways driven by changes in the abundance ratio of Serratia to other bacterial genera. Increased CD4 T cell numbers over the first year were associated with high Serratia abundance, pro-inflammatory innate cytokines, and metabolites that drive Th17 gene expression signatures and restoration of mucosal integrity. Subsequently, decreased Serratia abundance and downregulation of innate cytokines allowed re-establishment of systemic T cell homeostasis promoting restoration of Th1 and Th2 gene expression signatures. Analyses of three other geographically distinct cohorts of treated HIV infection established a more generalized principle that changes in diversity and composition of translocated microbial species influence systemic inflammation and consequently CD4 T cell recovery.

SUBMITTER: Nganou-Makamdop K

PROVIDER: S-EPMC8316372 | biostudies-literature | 2021 Jul

REPOSITORIES: biostudies-literature

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Translocated microbiome composition determines immunological outcome in treated HIV infection.

Nganou-Makamdop Krystelle K Talla Aarthi A Sharma Ashish Arunkumar AA Darko Sam S Ransier Amy A Laboune Farida F Chipman Jeffrey G JG Beilman Gregory J GJ Hoskuldsson Torfi T Fourati Slim S Schmidt Thomas E TE Arumugam Sahaana S Lima Noemia S NS Moon Damee D Callisto Samuel S Schoephoerster Jordan J Tomalka Jeffery J Mugyenyi Peter P Ssali Francis F Muloma Proscovia P Ssengendo Patrick P Leda Ana R AR Cheu Ryan K RK Flynn Jacob K JK Morou Antigoni A Brunet-Ratnasingham Elsa E Rodriguez Benigno B Lederman Michael M MM Kaufmann Daniel E DE Klatt Nichole R NR Kityo Cissy C Brenchley Jason M JM Schacker Timothy W TW Sekaly Rafick P RP Douek Daniel C DC

Cell 20210707 15

The impact of the microbiome on HIV disease is widely acknowledged although the mechanisms downstream of fluctuations in microbial composition remain speculative. We detected rapid, dynamic changes in translocated microbial constituents during two years after cART initiation. An unbiased systems biology approach revealed two distinct pathways driven by changes in the abundance ratio of Serratia to other bacterial genera. Increased CD4 T cell numbers over the first year were associated with high ...[more]

PMID: 34237254

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Project description:BackgroundMicrobes play a role in their host's fundamental ecological, chemical, and physiological processes. Host life-history traits from defence to growth are therefore determined not only by the abiotic environment and genotype but also by microbiota composition. However, the relative importance and interactive effects of these factors may vary between organisms. Such connections remain particularly elusive in Lepidoptera, which have been argued to lack a permanent microbiome and have microbiota primarily determined by their diet and environment. We tested the microbiome specificity and its influence on life-history traits of two colour genotypes of the wood tiger moth (Arctia plantaginis) that differ in several traits, including growth. All individuals were grown in the laboratory for several generations with standardized conditions. We analyzed the bacterial community of the genotypes before and after a reciprocal frass (i.e., larval faeces) transplantation and followed growth rate, pupal mass, and the production of defensive secretion.ResultsAfter transplantation, the fast-growing genotype grew significantly slower compared to the controls, but the slow-growing genotype did not change its growth rate. The frass transplant also increased the volume of defensive secretions in the fast-growing genotype but did not affect pupal mass. Overall, the fast-growing genotype appeared more susceptible to the transplantation than the slow-growing genotype. Microbiome differences between the genotypes strongly suggest genotype-based selective filtering of bacteria from the diet and environment. A novel cluster of insect-associated Erysipelotrichaceae was exclusive to the fast-growing genotype, and specific Enterococcaceae were characteristic to the slow-growing genotype. These Enterococcaceae became more prevalent in the fast-growing genotype after the transplant, which suggests that a slower growth rate is potentially related to their presence.ConclusionsWe show that reciprocal frass transplantation can reverse some genotype-specific life-history traits in a lepidopteran host. The results indicate that genotype-specific selective filtering can fine-tune the bacterial community at specific life stages and tissues like the larval frass, even against a background of a highly variable community with stochastic assembly. Altogether, our findings suggest that the host's genotype can influence its susceptibility to being colonized by microbiota, impacting key life-history traits.

Dataset Information

Translocated microbiome composition determines immunological outcome in treated HIV infection.

Publications

Translocated microbiome composition determines immunological outcome in treated HIV infection.

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