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1. Immune Gene Expression Covaries with Gut Microbiome Composition in Stickleback

   https://doi.org/10.1128/mBio.00145-21  

   Fuess, Lauren E.; den Haan, Stijn; Ling, Fei; Weber, Jesse N.; Steinel, Natalie C.; Bolnick, Daniel I. (January 2021, mBio)

   Rawls, John F.; McFall-Ngai, Margaret J. (Ed.)

   ABSTRACT Commensal microbial communities have immense effects on their vertebrate hosts, contributing to a number of physiological functions, as well as host fitness. In particular, host immunity is strongly linked to microbiota composition through poorly understood bi-directional links. Gene expression may be a potential mediator of these links between microbial communities and host function. However, few studies have investigated connections between microbiota composition and expression of host immune genes in complex systems. Here, we leverage a large study of laboratory-raised fish from the species Gasterosteus aculeatus (three-spined stickleback) to document correlations between gene expression and microbiome composition. First, we examined correlations between microbiome alpha diversity and gene expression. Our results demonstrate robust positive associations between microbial alpha diversity and expression of host immune genes. Next, we examined correlations between host gene expression and abundance of microbial taxa. We identified 15 microbial families that were highly correlated with host gene expression. These families were all tightly correlated with host expression of immune genes and processes, falling into one of three categories—those positively correlated, negatively correlated, and neutrally related to immune processes. Furthermore, we highlight several important immune processes that are commonly associated with the abundance of these taxa, including both macrophage and B cell functions. Further functional characterization of microbial taxa will help disentangle the mechanisms of the correlations described here. In sum, our study supports prevailing hypotheses of intimate links between host immunity and gut microbiome composition. IMPORTANCE Here, we document associations between host gene expression and gut microbiome composition in a nonmammalian vertebrate species. We highlight associations between expression of immune genes and both microbiome diversity and abundance of specific microbial taxa. These findings support other findings from model systems which have suggested that gut microbiome composition and host immunity are intimately linked. Furthermore, we demonstrate that these correlations are truly systemic; the gene expression detailed here was collected from an important fish immune organ (the head kidney) that is anatomically distant from the gut. This emphasizes the systemic impact of connections between gut microbiota and host immune function. Our work is a significant advancement in the understanding of immune-microbiome links in nonmodel, natural systems. 

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2. Large Comparative Analyses of Primate Body Site Microbiomes Indicate that the Oral Microbiome Is Unique among All Body Sites and Conserved among Nonhuman Primates

   https://doi.org/10.1128/spectrum.01643-21  

   Asangba, Abigail E.; Mugisha, Lawrence; Rukundo, Joshua; Lewis, Rebecca J.; Halajian, Ali; Cortés-Ortiz, Liliana; Junge, Randall E.; Irwin, Mitchell T.; Karlson, Johan; Perkin, Andrew; et al (June 2022, Microbiology Spectrum)

   Kormas, Konstantinos Aristomenis (Ed.)

   ABSTRACT The study of the mammalian microbiome serves as a critical tool for understanding host-microbial diversity and coevolution and the impact of bacterial communities on host health. While studies of specific microbial systems (e.g., in the human gut) have rapidly increased, large knowledge gaps remain, hindering our understanding of the determinants and levels of variation in microbiomes across multiple body sites and host species. Here, we compare microbiome community compositions from eight distinct body sites among 17 phylogenetically diverse species of nonhuman primates (NHPs), representing the largest comparative study of microbial diversity across primate host species and body sites. Analysis of 898 samples predominantly acquired in the wild demonstrated that oral microbiomes were unique in their clustering, with distinctive divergence from all other body site microbiomes. In contrast, all other body site microbiomes clustered principally by host species and differentiated by body site within host species. These results highlight two key findings: (i) the oral microbiome is unique compared to all other body site microbiomes and conserved among diverse nonhuman primates, despite their considerable dietary and phylogenetic differences, and (ii) assessments of the determinants of host-microbial diversity are relative to the level of the comparison (i.e., intra-/inter-body site, -host species, and -individual), emphasizing the need for broader comparative microbial analyses across diverse hosts to further elucidate host-microbial dynamics, evolutionary and biological patterns of variation, and implications for human-microbial coevolution. IMPORTANCE The microbiome is critical to host health and disease, but much remains unknown about the determinants, levels, and evolution of host-microbial diversity. The relationship between hosts and their associated microbes is complex. Most studies to date have focused on the gut microbiome; however, large gaps remain in our understanding of host-microbial diversity, coevolution, and levels of variation in microbiomes across multiple body sites and host species. To better understand the patterns of variation and evolutionary context of host-microbial communities, we conducted one of the largest comparative studies to date, which indicated that the oral microbiome was distinct from the microbiomes of all other body sites and convergent across host species, suggesting conserved niche specialization within the Primates order. We also show the importance of host species differences in shaping the microbiome within specific body sites. This large, comparative study contributes valuable information on key patterns of variation among hosts and body sites, with implications for understanding host-microbial dynamics and human-microbial coevolution. 

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3. The gut bacterial microbiome of the Threeridge mussel, Amblema plicata , varies between rivers but shows a consistent core community

   https://doi.org/10.1111/fwb.13905  

   Lawson, Lauren A.; Atkinson, Carla L.; Jackson, Colin R. (March 2022, Freshwater Biology)

   Abstract Freshwater mussels are important for nutrient cycling and ecosystem health as they filter feed on their surrounding water. This filter feeding makes these bivalves especially sensitive to conditions in their environment. Gut microbial communities (microbiomes) have been recognised as important to both host organism and ecosystem health; however, how freshwater mussel microbiomes are organised and influenced is unclear.In this study, the gut bacterial microbiome of Threeridge mussel,Amblema plicata, was compared across two river basins, five rivers, and nine local sites in the south‐eastern U.S.A. Mussel gut tissue was dissected, DNA extracted, and the microbiome characterised by high throughput sequencing of the V4 region of the 16S ribosomal RNA gene.Planctomycetes, Firmicutes, and Cyanobacteria were the most common bacterial phyla within the guts of all sampledA.plicata. However, the relative abundances of these major bacterial phyla differed between mussels sampled from different rivers and river basins, as did the relative abundance of specific bacterial operational taxonomic units (OTUs). Despite these differences, a core microbiome was identified across all mussels, with eight OTUs being consistent members of theA.plicatamicrobiome at all sites, the most abundant OTU identifying as a member of the family Planctomycetaceae. Geographic distance between sites was not correlated with similarity in the structure of the gut microbiome, which was more related to site physicochemistry.Overall, these results suggest that while physicochemical conditions affect the composition of transient bacteria in the Threeridge mussel gut microbiome, the core microbiome is largely unaffected, and a portion of theA.plicatamicrobiome is retained regardless of the river system.How long transient bacteria remain in the gut, and to what extent these transient microbes aid in host function is still unknown. Core microbiota have been found to aid in multiple functions within animal hosts, and within freshwater mussels this core microbiome may aid in nutrient processing and cycling. Therefore, it is important to look at both transient and core microbes when studying the structure of freshwater invertebrate microbiomes. 

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4. Taxonomic, Genomic, and Functional Variation in the Gut Microbiomes of Wild Spotted Hyenas Across 2 Decades of Study

   https://doi.org/10.1128/msystems.00965-22  

   Rojas, Connie A.; Holekamp, Kay E.; Viladomat Jasso, Mariette; Souza, Valeria; Eisen, Jonathan A.; Theis, Kevin R. (January 2022, mSystems)

   Hird, Sarah M. (Ed.)

   The gut microbiome provides vital functions for mammalian hosts, yet research on its variability and function across adult life spans and multiple generations is limited in large mammalian carnivores. Here, we used 16S rRNA gene and metagenomic high-throughput sequencing to profile the bacterial taxonomic composition, genomic diversity, and metabolic function of fecal samples collected from 12 wild spotted hyenas ( Crocuta crocuta ) residing in the Masai Mara National Reserve, Kenya, over a 23-year period spanning three generations. The metagenomic data came from four of these hyenas and spanned two 2-year periods. With these data, we determined the extent to which host factors predicted variation in the gut microbiome and identified the core microbes present in the guts of hyenas. We also investigated novel genomic diversity in the mammalian gut by reporting the first metagenome-assembled genomes (MAGs) for hyenas. We found that gut microbiome taxonomic composition varied temporally, but despite this, a core set of 14 bacterial genera were identified. The strongest predictors of the microbiome were host identity and age, suggesting that hyenas possess individualized microbiomes and that these may change with age during adulthood. The gut microbiome functional profiles of the four adult hyenas were also individual specific and were associated with prey abundance, indicating that the functions of the gut microbiome vary with host diet. We recovered 149 high-quality MAGs from the hyenas’ guts; some MAGs were classified as taxa previously reported for other carnivores, but many were novel and lacked species-level matches to genomes in existing reference databases. IMPORTANCE There is a gap in knowledge regarding the genomic diversity and variation of the gut microbiome across a host’s life span and across multiple generations of hosts in wild mammals. Using two types of sequencing approaches, we found that although gut microbiomes were individualized and temporally variable among hyenas, they correlated similarly to large-scale changes in the ecological conditions experienced by their hosts. We also recovered 149 high-quality MAGs from the hyena gut, greatly expanding the microbial genome repertoire known for hyenas, carnivores, and wild mammals in general. Some MAGs came from genera abundant in the gastrointestinal tracts of canid species and other carnivores, but over 80% of MAGs were novel and from species not previously represented in genome databases. Collectively, our novel body of work illustrates the importance of surveying the gut microbiome of nonmodel wild hosts, using multiple sequencing methods and computational approaches and at distinct scales of analysis. 

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5. The importance of host physical niches for the stability of gut microbiome composition

   https://doi.org/10.1098/rstb.2023.0066  

   Ludington, William B (May 2024, Philosophical Transactions of the Royal Society B: Biological Sciences)

   Gut bacteria are prevalent throughout the Metazoa and form complex microbial communities associated with food breakdown, nutrient provision and disease prevention. How hosts acquire and maintain a consistent bacterial flora remains mysterious even in the best-studied animals, including humans, mice, fishes, squid, bugs, worms and flies. This essay visits the evidence that hosts have co-evolved relationships with specific bacteria and that some of these relationships are supported by specialized physical niches that select, sequester and maintain microbial symbionts. Genetics approaches could uncover the mechanisms for recruiting and maintaining the stable and consistent members of the microbiome. This article is part of the theme issue ‘Sculpting the microbiome: how host factors determine and respond to microbial colonization’. 

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