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1. 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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2. A ridge-to-reef ecosystem microbial census reveals environmental reservoirs for animal and plant microbiomes

   https://doi.org/10.1073/pnas.2204146119  

   Amend, Anthony S.; Swift, Sean O.; Darcy, John L.; Belcaid, Mahdi; Nelson, Craig E.; Buchanan, Joshua; Cetraro, Nicolas; Fraiola, Kauaoa M.; Frank, Kiana; Kajihara, Kacie; et al (August 2022, Proceedings of the National Academy of Sciences)

   Microbes are found in nearly every habitat and organism on the planet, where they are critical to host health, fitness, and metabolism. In most organisms, few microbes are inherited at birth; instead, acquiring microbiomes generally involves complicated interactions between the environment, hosts, and symbionts. Despite the criticality of microbiome acquisition, we know little about where hosts’ microbes reside when not in or on hosts of interest. Because microbes span a continuum ranging from generalists associating with multiple hosts and habitats to specialists with narrower host ranges, identifying potential sources of microbial diversity that can contribute to the microbiomes of unrelated hosts is a gap in our understanding of microbiome assembly. Microbial dispersal attenuates with distance, so identifying sources and sinks requires data from microbiomes that are contemporary and near enough for potential microbial transmission. Here, we characterize microbiomes across adjacent terrestrial and aquatic hosts and habitats throughout an entire watershed, showing that the most species-poor microbiomes are partial subsets of the most species-rich and that microbiomes of plants and animals are nested within those of their environments. Furthermore, we show that the host and habitat range of a microbe within a single ecosystem predicts its global distribution, a relationship with implications for global microbial assembly processes. Thus, the tendency for microbes to occupy multiple habitats and unrelated hosts enables persistent microbiomes, even when host populations are disjunct. Our whole-watershed census demonstrates how a nested distribution of microbes, following the trophic hierarchies of hosts, can shape microbial acquisition. 

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3. How host-microbiome/holobiont evolution depends on whether the microbiome affects host lifespan or fecundity

   https://doi.org/10.1093/jeb/voae127  

   Brown, Alexandra L; Koskella, Britt; Boots, Mike (January 2025, Journal of Evolutionary Biology)

   Li_Richter, Xiang-Yi; Jain, Kavita (Ed.)

   Abstract There is overwhelming evidence that the microbiome can be important to host physiology and fitness. As such, there is interest in and some theoretical work on understanding when hosts and microbiomes (co)evolve so that microbes benefit hosts and hosts favour beneficial microbes. However, the outcome of evolution likely depends on how microbes benefit hosts. Here, we use adaptive dynamics to investigate how host and symbiont evolution depend on whether symbionts increase host lifespan or host reproduction in a simple model of host and symbiont dynamics. In addition, we investigate 2 ways hosts release (and transmit) symbionts: by releasing symbionts steadily during their lifetime or by releasing them at reproduction, potentially increasing symbionts’ chances of infecting the host’s offspring. The former is strict horizontal transmission, whereas the latter is also a form of indirect or “pseudovertical” transmission. Our first key result is that the evolution of symbionts that benefit host fecundity requires pseudovertical transmission, while the evolution of symbionts that benefit host lifespan does not. Furthermore, our second key result is that when investing in host benefits is costly to the free-living symbiont stage, intermediate levels of pseudovertical transmission are needed for selection to favour beneficial symbionts. This is true regardless of fitness effects because release at reproduction increases the free-living symbiont population, which increases competition for hosts. Consequently, hosts could evolve away from traits that favour beneficial symbionts. Generally, our work emphasizes the importance of different forms of vertical transmission and fitness benefits in host, microbiome, and holobiont evolution as highlighted by our prediction that the evolution of fecundity-increasing symbionts requires parent-to-offspring transmission. 

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4. Trait-Based Comparison of Coral and Sponge Microbiomes

   https://doi.org/10.1038/s41598-020-59320-9  

   Fiore, Cara L.; Jarett, Jessica K.; Steinert, Georg; Lesser, Michael P. (February 2020, Scientific Reports)

   Abstract Corals and sponges harbor diverse microbial communities that are integral to the functioning of the host. While the taxonomic diversity of their microbiomes has been well-established for corals and sponges, their functional roles are less well-understood. It is unclear if the similarities of symbiosis in an invertebrate host would result in functionally similar microbiomes, or if differences in host phylogeny and environmentally driven microhabitats within each host would shape functionally distinct communities. Here we addressed this question, using metatranscriptomic and 16S rRNA gene profiling techniques to compare the microbiomes of two host organisms from different phyla. Our results indicate functional similarity in carbon, nitrogen, and sulfur assimilation, and aerobic nitrogen cycling. Additionally, there were few statistical differences in pathway coverage or abundance between the two hosts. For example, we observed higher coverage of phosphonate and siderophore metabolic pathways in the star coral,Montastraea cavernosa, while there was higher coverage of chloroalkane metabolism in the giant barrel sponge,Xestospongia muta. Higher abundance of genes associated with carbon fixation pathways was also observed inM. cavernosa, while inX. mutathere was higher abundance of fatty acid metabolic pathways. Metagenomic predictions based on 16S rRNA gene profiling analysis were similar, and there was high correlation between the metatranscriptome and metagenome predictions for both hosts. Our results highlight several metabolic pathways that exhibit functional similarity in these coral and sponge microbiomes despite the taxonomic differences between the two microbiomes, as well as potential specialization of some microbially based metabolism within each host. 

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5. Phylosymbiosis shapes skin bacterial communities and pathogen-protective function in Appalachian salamanders

   https://doi.org/10.1093/ismejo/wrae104  

   Osborne, Owen_G; Jiménez, Randall_R; Byrne, Allison_Q; Gratwicke, Brian; Ellison, Amy; Muletz-Wolz, Carly_R (June 2024, The ISME Journal)

   Abstract Phylosymbiosis is an association between host-associated microbiome composition and host phylogeny. This pattern can arise via the evolution of host traits, habitat preferences, diets, and the co-diversification of hosts and microbes. Understanding the drivers of phylosymbiosis is vital for modelling disease-microbiome interactions and manipulating microbiomes in multi-host systems. This study quantifies phylosymbiosis in Appalachian salamander skin in the context of infection by the fungal pathogen Batrachochytrium dendrobatidis (Bd), while accounting for environmental microbiome exposure. We sampled ten salamander species representing >150M years of divergence, assessed their Bd infection status, and analysed their skin and environmental microbiomes. Our results reveal a significant signal of phylosymbiosis, whereas the local environmental pool of microbes, climate, geography, and Bd infection load had a smaller impact. Host-microbe co-speciation was not evident, indicating that the effect stems from the evolution of host traits influencing microbiome assembly. Bd infection is correlated with host phylogeny and the abundance of Bd-inhibitory bacterial strains, suggesting that the long-term evolutionary dynamics between salamander hosts and their skin microbiomes affect the present-day distribution of the pathogen, along with habitat-linked exposure risk. Five Bd-inhibitory bacterial strains showed unusual generalism: occurring in most host species and habitats. These generalist strains may enhance the likelihood of probiotic manipulations colonising and persisting on hosts. Our results underscore the substantial influence of host-microbiome eco-evolutionary dynamics on environmental health and disease outcomes. 

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