Gut Immune Responses and Evolution of the Gut Microbiome-a Hypothesis

Overview

Journal Discov Immunol

Specialty Allergy & Immunology

Date 2024 Apr 3

PMID 38567055

Authors

Mark Viney

Louise Cheynel

Affiliations

Soon will be listed here.

Abstract

The gut microbiome is an assemblage of microbes that have profound effects on their hosts. The composition of the microbiome is affected by bottom-up, among-taxa interactions and by top-down, host effects, which includes the host immune response. While the high-level composition of the microbiome is generally stable over time, component strains and genotypes will constantly be evolving, with both bottom-up and top-down effects acting as selection pressures, driving microbial evolution. Secretory IgA is a major feature of the gut's adaptive immune response, and a substantial proportion of gut bacteria are coated with IgA, though the effect of this on bacteria is unclear. Here we hypothesize that IgA binding to gut bacteria is a selection pressure that will drive the evolution of IgA-bound bacteria, so that they will have a different evolutionary trajectory than those bacteria not bound by IgA. We know very little about the microbiome of wild animals and even less about their gut immune responses, but it must be a priority to investigate this hypothesis to understand if and how host immune responses contribute to microbiome evolution.

References

Goodrich J, Davenport E, Beaumont M, Jackson M, Knight R, Ober C . Genetic Determinants of the Gut Microbiome in UK Twins. Cell Host Microbe. 2016; 19(5):731-43. PMC: 4915943. DOI: 10.1016/j.chom.2016.04.017. View

Ellegaard K, Engel P . Beyond 16S rRNA Community Profiling: Intra-Species Diversity in the Gut Microbiota. Front Microbiol. 2016; 7:1475. PMC: 5030217. DOI: 10.3389/fmicb.2016.01475. View

Groussin M, Poyet M, Sistiaga A, Kearney S, Moniz K, Noel M . Elevated rates of horizontal gene transfer in the industrialized human microbiome. Cell. 2021; 184(8):2053-2067.e18. DOI: 10.1016/j.cell.2021.02.052. View

Belkaid Y, Hand T . Role of the microbiota in immunity and inflammation. Cell. 2014; 157(1):121-41. PMC: 4056765. DOI: 10.1016/j.cell.2014.03.011. View

Muir A, Bennett A, Smith H, Logunova L, Wolfenden A, Fenn J . The wild mouse bone marrow has a unique myeloid and lymphoid composition and phenotype. Discov Immunol. 2024; 2(1):kyad005. PMC: 10917185. DOI: 10.1093/discim/kyad005. View

Petrova V, Russell C . The evolution of seasonal influenza viruses. Nat Rev Microbiol. 2017; 16(1):60. DOI: 10.1038/nrmicro.2017.146. View

Ivanov I, de Llanos Frutos R, Manel N, Yoshinaga K, Rifkin D, Sartor R . Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe. 2008; 4(4):337-49. PMC: 2597589. DOI: 10.1016/j.chom.2008.09.009. View

Faith J, Guruge J, Charbonneau M, Subramanian S, Seedorf H, Goodman A . The long-term stability of the human gut microbiota. Science. 2013; 341(6141):1237439. PMC: 3791589. DOI: 10.1126/science.1237439. View

Huus K, Petersen C, Finlay B . Diversity and dynamism of IgA-microbiota interactions. Nat Rev Immunol. 2021; 21(8):514-525. DOI: 10.1038/s41577-021-00506-1. View

10.

Viney M . The gut microbiota of wild rodents: Challenges and opportunities. Lab Anim. 2018; 53(3):252-258. DOI: 10.1177/0023677218787538. View

11.

Donald K, Petersen C, Turvey S, Finlay B, Azad M . Secretory IgA: Linking microbes, maternal health, and infant health through human milk. Cell Host Microbe. 2022; 30(5):650-659. DOI: 10.1016/j.chom.2022.02.005. View

12.

Okai S, Usui F, Yokota S, Hori-I Y, Hasegawa M, Nakamura T . High-affinity monoclonal IgA regulates gut microbiota and prevents colitis in mice. Nat Microbiol. 2016; 1(9):16103. DOI: 10.1038/nmicrobiol.2016.103. View

13.

Lipsitch M, OHagan J . Patterns of antigenic diversity and the mechanisms that maintain them. J R Soc Interface. 2007; 4(16):787-802. PMC: 2394542. DOI: 10.1098/rsif.2007.0229. View

14.

Nakajima A, Vogelzang A, Maruya M, Miyajima M, Murata M, Son A . IgA regulates the composition and metabolic function of gut microbiota by promoting symbiosis between bacteria. J Exp Med. 2018; 215(8):2019-2034. PMC: 6080902. DOI: 10.1084/jem.20180427. View

15.

Suzuki T, Phifer-Rixey M, Mack K, Sheehan M, Lin D, Bi K . Host genetic determinants of the gut microbiota of wild mice. Mol Ecol. 2019; 28(13):3197-3207. PMC: 6660988. DOI: 10.1111/mec.15139. View

16.

Bar J, Leung J, Hansen C, Loke P, Hall A, Conour L . Strong effects of lab-to-field environmental transitions on the bacterial intestinal microbiota of Mus musculus are modulated by Trichuris murisinfection. FEMS Microbiol Ecol. 2020; 96(10). DOI: 10.1093/femsec/fiaa167. View

17.

Allen T, Altfeld M, Geer S, Kalife E, Moore C, OSullivan K . Selective escape from CD8+ T-cell responses represents a major driving force of human immunodeficiency virus type 1 (HIV-1) sequence diversity and reveals constraints on HIV-1 evolution. J Virol. 2005; 79(21):13239-49. PMC: 1262562. DOI: 10.1128/JVI.79.21.13239-13249.2005. View

18.

McLoughlin K, Schluter J, Rakoff-Nahoum S, Smith A, Foster K . Host Selection of Microbiota via Differential Adhesion. Cell Host Microbe. 2016; 19(4):550-9. DOI: 10.1016/j.chom.2016.02.021. View

19.

Barroso-Batista J, Sousa A, Lourenco M, Bergman M, Sobral D, Demengeot J . The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps. PLoS Genet. 2014; 10(3):e1004182. PMC: 3945185. DOI: 10.1371/journal.pgen.1004182. View

20.

Rollenske T, Burkhalter S, Muerner L, von Gunten S, Lukasiewicz J, Wardemann H . Parallelism of intestinal secretory IgA shapes functional microbial fitness. Nature. 2021; 598(7882):657-661. DOI: 10.1038/s41586-021-03973-7. View