Evolution of animal immunity in the light of beneficial symbioses

Hoang, Kim Le Mai; Stoy, Kayla S.

doi:10.1098/rstb.2019.0601

Cited by 50 publications

(52 citation statements)

References 138 publications

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“…Closely related hosts are potentially colonized by taxonomically similar microbes due to similarities in their morphology, anatomy, digestive physiologies, and immune system components [ 38 – 40 ]. Specifically, related hosts may possess similar antimicrobial peptides and toll-like receptors that serve to filter the same bacterial clades from the environment [ 41 , 42 ]. Closely related hosts may further develop immune tolerance via adaptive immunity to the same symbiotic, commensal, and transient microbes [ 41 , 42 ].…”

Section: Discussionmentioning

confidence: 99%

“…Specifically, related hosts may possess similar antimicrobial peptides and toll-like receptors that serve to filter the same bacterial clades from the environment [ 41 , 42 ]. Closely related hosts may further develop immune tolerance via adaptive immunity to the same symbiotic, commensal, and transient microbes [ 41 , 42 ]. Lastly, some closely related hosts may also possess similar social group structures and pathways for transmitting microbes among group-mates, thereby contributing to patterns of phylosymbiosis [ 43 – 46 ].…”

Section: Discussionmentioning

confidence: 99%

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Host phylogeny and host ecology structure the mammalian gut microbiota at different taxonomic scales

et al. 2021

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The gut microbiota is critical for host function. Among mammals, host phylogenetic relatedness and diet are strong drivers of gut microbiota structure, but one factor may be more influential than the other. Here, we used 16S rRNA gene sequencing to determine the relative contributions of host phylogeny and host diet in structuring the gut microbiotas of 11 herbivore species from 5 families living sympatrically in southwest Kenya. Herbivore species were classified as grazers, browsers, or mixed-feeders and dietary data (% C4 grasses in diet) were compiled from previously published sources. We found that herbivore gut microbiotas were highly species-specific, and that host taxonomy accounted for more variation in the gut microbiota (30%) than did host dietary guild (10%) or sample month (8%). Overall, similarity in the gut microbiota increased with host phylogenetic relatedness (r = 0.74) across the 11 species of herbivores, but among 7 closely related Bovid species, dietary %C4 grass values more strongly predicted gut microbiota structure (r = 0.64). Additionally, within bovids, host dietary guild explained more of the variation in the gut microbiota (17%) than did host species (12%). Lastly, while we found that the gut microbiotas of herbivores residing in southwest Kenya converge with those of distinct populations of conspecifics from central Kenya, fine-scale differences in the abundances of bacterial amplicon sequence variants (ASVs) between individuals from the two regions were also observed. Overall, our findings suggest that host phylogeny and taxonomy strongly structure the gut microbiota across broad host taxonomic scales, but these gut microbiotas can be further modified by host ecology (i.e., diet, geography), especially among closely related host species.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Host phylogeny and host ecology structure the mammalian gut microbiota at different taxonomic scales

et al. 2021

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“…Closely related hosts are potentially colonized by taxonomically similar microbes due to similarities in their morphology, anatomy, digestive physiologies, and immune system components [37, 38, 67]. Specifically, related hosts may possess similar antimicrobial peptides and toll-like receptors that serve to filter the same bacterial clades from the environment [68, 69]. Closely related hosts may further develop immune tolerance via adaptive immunity to the same symbiotic, commensal, and transient microbes [68, 69].…”

Section: Discussionmentioning

confidence: 99%

“…Specifically, related hosts may possess similar antimicrobial peptides and toll-like receptors that serve to filter the same bacterial clades from the environment [68, 69]. Closely related hosts may further develop immune tolerance via adaptive immunity to the same symbiotic, commensal, and transient microbes [68, 69]. Lastly, some phylogenetically related hosts may also possess similar social group structures and pathways for transmitting microbes among group-mates, thereby contributing to patterns of phylosymbiosis.…”

Section: Discussionmentioning

confidence: 99%

Host phylogeny and host ecology structure the mammalian gut microbiota at different taxonomic scales

Rojas

Ramírez‐Barahona

Holekamp

et al. 2020

Preprint

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The gut microbiota is critical for host function. Among mammals, host phylogenetic relatedness and diet are strong drivers of gut microbiota structure, but one factor may be more influential than the other. Here, we used 16S rRNA gene sequencing to determine the relative contributions of host phylogeny and host dietary guild in structuring the gut microbiotas of 11 herbivore species from 5 families living sympatrically in southwest Kenya. Herbivore species were classified as grazers, browsers, or mixed-feeders. We found that gut microbiotas were highly species-specific, and that host family accounted for more variation in the gut microbiota (35%) than did host dietary guild (14%). Overall, similarity among gut microbiotas increased with host phylogenetic relatedness (r=0.73), yet this relationship was not apparent among seven closely related Bovid host species (r=0.21 NS). In bovids, host dietary guild explained twice as much variation in the gut microbiota as did host species. Lastly, we found that the gut microbiotas of herbivores residing in southwest Kenya closely resemble those of conspecifics from central Kenya, suggesting that regardless of variability in host local habitat, hosts consistently provide microbes with similar niches for colonization. Overall, our findings suggest that host phylogeny may structure the gut microbiota at broad taxonomic scales, but that host ecology may be more influential in shaping the gut microbiotas of closely related host species.

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“…metabolites), or mediate indirect process such as T-cell polarization and the regulation of immune cell trafficking [18]. Commensal gut populations modulate hosts' immune responses, which in turn can modify the microbiota composition to maintain gut homeostasis [20,21]. Recently, polymorphisms located in immune genes associated with the abundance of microbial communities have been reported [22][23][24][25].…”

Section: Introductionmentioning

confidence: 99%

Leveraging host-genetics and gut microbiota to determine immunocompetence in pigs

Ramayo-Caldas

Zingaretti

Pérez-Pascual

et al. 2021

Preprint

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The aim of the present work was to identify microbial biomarkers linked to immunity traits and to characterize the contribution of host-genome and gut microbiota to the immunocompetence in healthy pigs. To achieve this goal, we undertook a combination of network, mixed model and microbial-wide association studies (MWAS) for 21 immunity traits and the relative abundance of gut bacterial communities in 389 pigs genotyped for 70K SNPs. The heritability (h2; proportion of phenotypic variance explained by the host genetics) and microbiability (m2; proportion of variance explained by the microbial composition) showed similar values for most of the analyzed immunity traits, except for both IgM and IgG in plasma that were dominated by the host genetics, and the haptoglobin in serum which was the trait with larger m2 (0.275) compared to h2 (0.138). Results from the MWAS suggested a polymicrobial nature of the immunocompetence in pigs and revealed associations between pigs gut microbiota composition and 15 of the analyzed traits. The lymphocytes phagocytic capacity (quantified as mean fluorescence) and the total number of monocytes in blood were the traits associated with the largest number of taxa (6 taxa). Among the associations identified by MWAS, 30% were confirmed by an information theory network approach. The strongest confirmed associations were between Fibrobacter and phagocytic capacity of lymphocytes (r=0.37), followed by correlations between Streptococcus and the percentage of phagocytic lymphocytes (r=-0.34) and between Megasphaera and serum concentration of haptoglobin (r=0.26). In the interaction network, Streptococcus and percentage of phagocytic lymphocytes were the keystone bacterial and immune-trait, respectively. Overall, our findings reveal an important connection between immunity traits and gut microbiota in pigs and highlight the need to consider both sources of information, host genome and microbial levels, to accurately characterize immunocompetence in pigs.

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Evolution of animal immunity in the light of beneficial symbioses

Cited by 50 publications

References 138 publications

Host phylogeny and host ecology structure the mammalian gut microbiota at different taxonomic scales

Host phylogeny and host ecology structure the mammalian gut microbiota at different taxonomic scales

Host phylogeny and host ecology structure the mammalian gut microbiota at different taxonomic scales

Leveraging host-genetics and gut microbiota to determine immunocompetence in pigs

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