Microbiome stability and structure is governed by host phylogeny over diet and geography in woodrats (Neotoma spp.)

2021 ◽  
Vol 118 (47) ◽  
pp. e2108787118
Author(s):  
Sara B. Weinstein ◽  
Rodolfo Martínez-Mota ◽  
Tess E. Stapleton ◽  
Dylan M. Klure ◽  
Robert Greenhalgh ◽  
...  

The microbiome is critical for host survival and fitness, but gaps remain in our understanding of how this symbiotic community is structured. Despite evidence that related hosts often harbor similar bacterial communities, it is unclear whether this pattern is due to genetic similarities between hosts or to common ecological selection pressures. Here, using herbivorous rodents in the genus Neotoma, we quantify how geography, diet, and host genetics, alongside neutral processes, influence microbiome structure and stability under natural and captive conditions. Using bacterial and plant metabarcoding, we first characterized dietary and microbiome compositions for animals from 25 populations, representing seven species from 19 sites across the southwestern United States. We then brought wild animals into captivity, reducing the influence of environmental variation. In nature, geography, diet, and phylogeny collectively explained ∼50% of observed microbiome variation. Diet and microbiome diversity were correlated, with different toxin-enriched diets selecting for distinct microbial symbionts. Although diet and geography influenced natural microbiome structure, the effects of host phylogeny were stronger for both wild and captive animals. In captivity, gut microbiomes were altered; however, responses were species specific, indicating again that host genetic background is the most significant predictor of microbiome composition and stability. In captivity, diet effects declined and the effects of host genetic similarity increased. By bridging a critical divide between studies in wild and captive animals, this work underscores the extent to which genetics shape microbiome structure and stability in closely related hosts.

Parasitology ◽  
1998 ◽  
Vol 117 (6) ◽  
pp. 563-569 ◽  
Author(s):  
J. A. JACKSON ◽  
R. C. TINSLEY ◽  
H. H. HINKEL

Adults of the monogenean genus Protopolystoma infecting Xenopus species occur in an extremely space-limited habitat, the urinary bladder. Xenopus wittei, from a population in Rwanda naturally infected with Protopolystoma fissilis and Protopolystoma simplicis, were exposed to reinfection in captivity (for 1–3 months post-capture) and then monitored in the laboratory for up to 5 months in transmission-free conditions. The two parasites co-occurred in individual bladders less frequently than expected if they were dispersed randomly. Distribution of bladder infections was significantly non-independent (n=157) and gravid worms of both species were never found in the same host. This pattern might be explained by interference competition between the parasites or by genetic differences in susceptibility within the host species, which is of allopolyploid origin. Other distributional data for sympatric polystomatid species pairs, including P. fissilis and P. ramulosus, show concurrent infections at frequencies consistent with random distributions (i.e. no evidence of interspecific competition or variability in species-specific susceptibility of the hosts). Interference between P. fissilis and P. simplicis (assuming host genetic factors are not involved) may therefore result from a mechanism specific to this species pair. Observations on infection turnover in captive hosts suggest that loss of adult worms may be related to the arrival of juveniles (of either species) in the urinary bladder. Ectopic infection of the host urinary ducts by adult and subadult P. fissilis was observed in some single-species infestations and may be density related. However, the use of an ectopic-site ‘refugium’ has never been observed in concurrent polystomatid infections.


2019 ◽  
Author(s):  
Petar Scepanovic ◽  
Flavia Hodel ◽  
Stanislas Mondot ◽  
Valentin Partula ◽  
Allyson Byrd ◽  
...  

ABSTRACTBackgroundThe gut microbiome is an important determinant of human health. Its composition has been shown to be influenced by multiple environmental factors and likely by host genetic variation. In the framework of the Milieu Intérieur Consortium, a total of 1,000 healthy individuals of western European ancestry, with a 1:1 sex ratio and evenly stratified across five decades of life (age 20 – 69), were recruited. We generated 16S ribosomal RNA profiles from stool samples for 858 participants. We investigated genetic and non-genetic factors that contribute to individual differences in fecal microbiome composition.ResultsAmong 110 demographic, clinical and environmental factors, 11 were identified as significantly correlated with α-diversity, ß-diversity or abundance of specific microbial communities in multivariable models. Age and blood alanine aminotransferase levels showed the strongest associations with microbiome diversity. In total, all non-genetic factors explained 16.4% of the variance. We then searched for associations between >5 million single nucleotide polymorphisms and the same indicators of fecal microbiome diversity, including the significant non-genetic factors as covariates. No genome-wide significant associations were identified after correction for multiple testing. A small fraction of previously reported associations between human genetic variants and specific taxa could be replicated in our cohort, while no replication was observed for any of the diversity metrics.ConclusionIn a well-characterized cohort of healthy individuals, we identified several non-genetic variables associated with fecal microbiome diversity. In contrast, host genetics only had a negligible influence. Demographic and environmental factors are thus the main contributors to fecal microbiome composition in healthy individuals.


2021 ◽  
Author(s):  
Alaina C Pfenning-Butterworth ◽  
Reilly Cooper ◽  
Clay Cressler

Host-associated microbial communities are impacted by external and within-host factors, i.e., diet and feeding behavior. For organisms known to have a circadian rhythm in feeding behavior, microbiome composition is likely impacted by the different rates of microbe introduction and removal across a daily cycle, in addition to any diet-induced changes in microbial interactions. Here, we measured feeding behavior and used 16S rRNA sequencing to compare the microbial community across a diel cycle in two distantly related species of Daphnia, that differ in their life history traits, to assess how daily feeding patterns impact microbiome composition. We find that Daphnia species reared under similar laboratory conditions have significantly different microbial communities. Additionally, we reveal that Daphnia have daily differences in their microbial composition that correspond with feeding behavior, such that there is greater microbiome diversity at night during the host's active feeding phase. These results highlight that zooplankton microbiomes are relatively distinct and are likely influenced by host phylogeny.


2020 ◽  
Vol 287 (1924) ◽  
pp. 20192367
Author(s):  
Jarrod J. Scott ◽  
Thomas C. Adam ◽  
Alain Duran ◽  
Deron E. Burkepile ◽  
Douglas B. Rasher

Microbes are ubiquitous throughout the world's oceans, yet the manner and extent of their influence on the ecology and evolution of large, mobile fauna remains poorly understood. Here, we establish the intestinal microbiome as a hidden, and potentially important, ‘functional trait’ of tropical herbivorous fishes—a group of large consumers critical to coral reef resilience. Using field observations, we demonstrate that five common Caribbean fish species display marked differences in where they feed and what they feed on. However, in addition to space use and feeding behaviour—two commonly measured functional traits—we find that interspecific trait differences are even more pronounced when considering the herbivore intestinal microbiome. Microbiome composition was highly species specific. Phylogenetic comparison of the dominant microbiome members to all known microbial taxa suggest that microbiomes are comprised of putative environmental generalists, animal-associates and fish specialists (resident symbionts), the latter of which mapped onto host phylogeny. These putative symbionts are most similar to—among all known microbes—those that occupy the intestines of ecologically and evolutionarily related herbivorous fishes in more distant ocean basins. Our findings therefore suggest that the intestinal microbiome may be an important functional trait among these large-bodied consumers.


Microbiome ◽  
2019 ◽  
Vol 7 (1) ◽  
Author(s):  
Petar Scepanovic ◽  
◽  
Flavia Hodel ◽  
Stanislas Mondot ◽  
Valentin Partula ◽  
...  

Abstract Background The gut microbiome is an important determinant of human health. Its composition has been shown to be influenced by multiple environmental factors and likely by host genetic variation. In the framework of the Milieu Intérieur Consortium, a total of 1000 healthy individuals of western European ancestry, with a 1:1 sex ratio and evenly stratified across five decades of life (age 20–69), were recruited. We generated 16S ribosomal RNA profiles from stool samples for 858 participants. We investigated genetic and non-genetic factors that contribute to individual differences in fecal microbiome composition. Results Among 110 demographic, clinical, and environmental factors, 11 were identified as significantly correlated with α-diversity, ß-diversity, or abundance of specific microbial communities in multivariable models. Age and blood alanine aminotransferase levels showed the strongest associations with microbiome diversity. In total, all non-genetic factors explained 16.4% of the variance. We then searched for associations between > 5 million single nucleotide polymorphisms and the same indicators of fecal microbiome diversity, including the significant non-genetic factors as covariates. No genome-wide significant associations were identified after correction for multiple testing. A small fraction of previously reported associations between human genetic variants and specific taxa could be replicated in our cohort, while no replication was observed for any of the diversity metrics. Conclusion In a well-characterized cohort of healthy individuals, we identified several non-genetic variables associated with fecal microbiome diversity. In contrast, host genetics only had a negligible influence. Demographic and environmental factors are thus the main contributors to fecal microbiome composition in healthy individuals. Trial registration ClinicalTrials.gov identifier NCT01699893


2021 ◽  
Author(s):  
Michael Oersted ◽  
Erika Yashiro ◽  
Ary A Hoffmann ◽  
Torsten Nygaard Kristensen

It is becoming increasingly clear that microbial symbionts influence key aspects of their host's fitness, and vice versa. This may fundamentally change our thinking about how microbes and hosts interact in influencing fitness and adaptation to changing environments. Here we explore how reductions in population size commonly experienced by threatened species influence microbiome diversity. Fitness consequences of such reductions are normally interpreted in terms of a loss of genetic variation and increase in inbreeding depression due to a loss of heterozygosity. However, fitness effects might also be mediated through microbiome diversity, e.g. if functionally important microbes are lost. Here we utilise Drosophila melanogaster lines with different histories of population bottlenecks to explore these questions. The lines were phenotyped for egg-to-adult viability and their genomes sequenced to estimate genetic variation. The bacterial 16S rRNA gene was amplified in these lines to investigate microbial diversity. We found that 1) host population bottlenecks constrained microbiome richness and diversity, 2) core microbiomes of hosts with low genetic variation were constituted from subsets of microbiomes found in flies with higher genetic variation, 3) both microbiome diversity and host genetic variation contributed to host population fitness, 4) connectivity and robustness of bacterial networks increased with higher host genetic variation, and 5) reduced microbial diversity is associated with weaker evolutionary responses in stressful environments. These findings suggest that population bottlenecks reduce hologenomic variation (in combined host and microbial genomes). Thus while the current biodiversity crisis focuses on population sizes and genetic variation of eukaryotes, an additional focal point should be the microbial diversity carried by the eukaryotes, which in turn may influence host fitness and adaptability with consequences for the persistence of populations.


Microbiome ◽  
2021 ◽  
Vol 9 (1) ◽  
Author(s):  
Antonio Reverter ◽  
Maria Ballester ◽  
Pamela A. Alexandre ◽  
Emilio Mármol-Sánchez ◽  
Antoni Dalmau ◽  
...  

Abstract Background Analyses of gut microbiome composition in livestock species have shown its potential to contribute to the regulation of complex phenotypes. However, little is known about the host genetic control over the gut microbial communities. In pigs, previous studies are based on classical “single-gene-single-trait” approaches and have evaluated the role of host genome controlling gut prokaryote and eukaryote communities separately. Results In order to determine the ability of the host genome to control the diversity and composition of microbial communities in healthy pigs, we undertook genome-wide association studies (GWAS) for 39 microbial phenotypes that included 2 diversity indexes, and the relative abundance of 31 bacterial and six commensal protist genera in 390 pigs genotyped for 70 K SNPs. The GWAS results were processed through a 3-step analytical pipeline comprised of (1) association weight matrix; (2) regulatory impact factor; and (3) partial correlation and information theory. The inferred gene regulatory network comprised 3561 genes (within a 5 kb distance from a relevant SNP–P < 0.05) and 738,913 connections (SNP-to-SNP co-associations). Our findings highlight the complexity and polygenic nature of the pig gut microbial ecosystem. Prominent within the network were 5 regulators, PRDM15, STAT1, ssc-mir-371, SOX9 and RUNX2 which gathered 942, 607, 588, 284 and 273 connections, respectively. PRDM15 modulates the transcription of upstream regulators of WNT and MAPK-ERK signaling to safeguard naive pluripotency and regulates the production of Th1- and Th2-type immune response. The signal transducer STAT1 has long been associated with immune processes and was recently identified as a potential regulator of vaccine response to porcine reproductive and respiratory syndrome. The list of regulators was enriched for immune-related pathways, and the list of predicted targets includes candidate genes previously reported as associated with microbiota profile in pigs, mice and human, such as SLIT3, SLC39A8, NOS1, IL1R2, DAB1, TOX3, SPP1, THSD7B, ELF2, PIANP, A2ML1, and IFNAR1. Moreover, we show the existence of host-genetic variants jointly associated with the relative abundance of butyrate producer bacteria and host performance. Conclusions Taken together, our results identified regulators, candidate genes, and mechanisms linked with microbiome modulation by the host. They further highlight the value of the proposed analytical pipeline to exploit pleiotropy and the crosstalk between bacteria and protists as significant contributors to host-microbiome interactions and identify genetic markers and candidate genes that can be incorporated in breeding program to improve host-performance and microbial traits.


2021 ◽  
Vol 9 ◽  
Author(s):  
Francesca De Martini ◽  
Nicole L. Coots ◽  
Daniel E. Jasso-Selles ◽  
Jordyn Shevat ◽  
Alison Ravenscraft ◽  
...  

The eukaryotic microbiome of “lower” termites is highly stable and host-specific. This is due to the mutually obligate nature of the symbiosis and the direct inheritance of protists by proctodeal trophallaxis. However, vertical transmission is occasionally imperfect, resulting in daughter colonies that lack one or more of the expected protist species. This phenomenon could conceivably lead to regional differences in protist community composition within a host species. Here, we have characterized the protist symbiont community of Heterotermes tenuis (Hagen) (Blattodea: Rhinotermitidae) from samples spanning South and Central America. Using light microscopy, single cell isolation, and amplicon sequencing, we report eight species-level protist phylotypes belonging to four genera in the phylum Parabasalia. The diversity and distribution of each phylotype’s 18S rRNA amplicon sequence variants (ASVs) mostly did not correlate with geographical or host genetic distances according to Mantel tests, consistent with the lack of correlation we observed between host genetic and geographical distances. However, the ASV distances of Holomastigotoides Ht3 were significantly correlated with geography while those of Holomastigotoides Ht1 were significantly correlated with host phylogeny. These results suggest mechanisms by which termite-associated protist species may diversify independently of each other and of their hosts, shedding light on the coevolutionary dynamics of this important symbiosis.


mSystems ◽  
2020 ◽  
Vol 5 (4) ◽  
Author(s):  
Supriya D. Mehta ◽  
Drew R. Nannini ◽  
Fredrick Otieno ◽  
Stefan J. Green ◽  
Walter Agingu ◽  
...  

ABSTRACT Bacterial vaginosis (BV) affects 20% of women worldwide and is associated with adverse reproductive health outcomes and increased risk for HIV. Typically, BV represents a shift in the vaginal microbiome from one that is dominated by Lactobacillus to one that is diverse. Persistent racial differences in BV and diverse vaginal microbiome composition overlap with racial disparities in risks for HIV and sexually transmitted infection, especially among women of African descent. Risk factors for BV and nonoptimal vaginal microbiome include sexual practices, yet racial differences persist when adjusted for behavioral factors, suggesting a host genetic component. Here, we perform a genome-wide association study on vaginal microbiome traits in Kenyan women. Linear regression and logistic regression were performed, adjusting for age and principal components of genetic ancestry, to evaluate the association between Lactobacillus crispatus, Lactobacillus iners, Gardnerella vaginalis, Shannon diversity index, and community state type (CST) with host genetic single nucleotide polymorphisms (SNPs). We identified novel genomic loci associated with the vaginal microbiome traits, though no SNP reached genome-wide significance. During pathway enrichment analysis, Toll-like receptors (TLRs), cytokine production, and other components of innate immune response were associated with L. crispatus, L. iners, and CST. Multiple previously reported genomic loci were replicated, including IL-8 (Shannon, CST), TIRAP (L. iners, Shannon), TLR2 (Shannon, CST), MBL2 (L. iners, G. vaginalis, CST), and MYD88 (L. iners, Shannon). These genetic associations suggest a role for the innate immune system and cell signaling in vaginal microbiome composition and susceptibility to nonoptimal vaginal microbiome. IMPORTANCE Globally, bacterial vaginosis (BV) is a common condition in women. BV is associated with poorer reproductive health outcomes and HIV risk. Typically, BV represents a shift in the vaginal microbiome from one that is dominated by Lactobacillus to one that is diverse. Despite many women having similar exposures, the prevalence of BV and nonoptimal vaginal microbiome is increased for women of African descent, suggesting a possible role for host genetics. We conducted a genome-wide association study of important vaginal microbiome traits in Kenyan women. We identified novel genetic loci and biological pathways related to mucosal immunity, cell signaling, and infection that were associated with vaginal microbiome traits; we replicated previously reported loci associated with mucosal immune response. These results provide insight into potential host genetic influences on vaginal microbiome composition and can guide larger longitudinal studies, with genetic and functional comparison across microbiome sites within individuals and across populations.


Sign in / Sign up

Export Citation Format

Share Document