Dataset Information

The Relationship Between Microbiomes and Selective Regimes in the Sponge Genus Ircinia.

ABSTRACT: Sponges are often densely populated by microbes that benefit their hosts through nutrition and bioactive secondary metabolites; however, sponges must simultaneously contend with the toxicity of microbes and thwart microbial overgrowth. Despite these fundamental tenets of sponge biology, the patterns of selection in the host sponges' genomes that underlie tolerance and control of their microbiomes are still poorly understood. To elucidate these patterns of selection, we performed a population genetic analysis on multiple species of Ircinia from Belize, Florida, and Panama using an F _ST -outlier approach on transcriptome-annotated RADseq loci. As part of the analysis, we delimited species boundaries among seven growth forms of Ircinia. Our analyses identified balancing selection in immunity genes that have implications for the hosts' tolerance of high densities of microbes. Additionally, our results support the hypothesis that each of the seven growth forms constitutes a distinct Ircinia species that is characterized by a unique microbiome. These results illuminate the evolutionary pathways that promote stable associations between host sponges and their microbiomes, and that potentially facilitate ecological divergence among Ircinia species.

SUBMITTER: Kelly JB

PROVIDER: S-EPMC7990798 | biostudies-literature | 2021

REPOSITORIES: biostudies-literature

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The Relationship Between Microbiomes and Selective Regimes in the Sponge Genus <i>Ircinia</i>.

Kelly Joseph B JB Carlson David E DE Low Jun Siong JS Rice Tyler T Thacker Robert W RW

Frontiers in microbiology 20210311

Sponges are often densely populated by microbes that benefit their hosts through nutrition and bioactive secondary metabolites; however, sponges must simultaneously contend with the toxicity of microbes and thwart microbial overgrowth. Despite these fundamental tenets of sponge biology, the patterns of selection in the host sponges' genomes that underlie tolerance and control of their microbiomes are still poorly understood. To elucidate these patterns of selection, we performed a population gen ...[more]

PMID: 33776953

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Project description:BackgroundAlthough the vaginal and urinary microbiomes have been increasingly well-characterized in health and disease, few have described the relationship between these neighboring environments. Elucidating this relationship has implications for understanding how manipulation of the vaginal microbiome may affect the urinary microbiome and treatment of common urinary conditions.ObjectiveTo describe the relationship between urinary and vaginal microbiomes using 16S rRNA gene sequencing. We hypothesized that the composition of the urinary and vaginal microbiomes would be significantly associated, with similarities in predominant taxa.Study designThis multicenter study collected vaginal swabs and catheterized urine samples from 186 women with mixed urinary incontinence enrolled in a parent study and 84 similarly aged controls. Investigators decided a priori that if vaginal and/or urinary microbiomes differed between continent and incontinent women, the groups would be analyzed separately; if similar, samples from continent and incontinent women would be pooled and analyzed together. A central laboratory sequenced variable regions 1-3 (v1-3) and characterized bacteria to the genus level. Operational taxonomic unit abundance was described for paired vaginal and urine samples. Pearson's correlation characterized the relationship between individual operational taxonomic units of paired samples. Canonical correlation analysis evaluated the association between clinical variables (including mixed urinary incontinence and control status) and vaginal and urinary operational taxonomic units, using the Canonical correlation analysis function in the Vegan package (R version 3.5). Linear discriminant analysis effect size was used to find taxa that discriminated between vaginal and urinary samples.ResultsUrinary and vaginal samples were collected from 212 women (mean age 53±11 years) and results from 197 paired samples were available for analysis. As operational taxonomic units in mixed urinary incontinence and control samples were related in canonical correlation analysis and since taxa did not discriminate between mixed urinary incontinence or controls in either vagina or urine, mixed urinary incontinence and control samples were pooled for further analysis. Canonical correlation analysis of vaginal and urinary samples indicated that that 60 of the 100 most abundant operational taxonomic units in the samples largely overlapped. Lactobacillus was the most abundant genus in both urine and vagina (contributing on average 53% to an individual's urine sample and 64% to an individual's vaginal sample) (Pearson correlation r=0.53). Although less abundant than Lactobacillus, other bacteria with high Pearson correlation coefficients also commonly found in vagina and urine included: Gardnerella (r=0.70), Prevotella (r=0.64), and Ureaplasma (r=0.50). Linear discriminant analysis effect size analysis identified Tepidimonas and Flavobacterium as bacteria that distinguished the urinary environment for both mixed urinary incontinence and controls as these bacteria were absent in the vagina (Tepidimonas effect size 2.38, P<.001, Flavobacterium effect size 2.15, P<.001). Although Lactobacillus was the most abundant bacteria in both urine and vagina, it was more abundant in the vagina (linear discriminant analysis effect size effect size 2.72, P<.001).ConclusionSignificant associations between vaginal and urinary microbiomes were demonstrated, with Lactobacillus being predominant in both urine and vagina. Abundance of other bacteria also correlated highly between the vagina and urine. This inter-relatedness has implications for studying manipulation of the urogenital microbiome in treating conditions such as urgency urinary incontinence and urinary tract infections.

Project description:BackgroundMarine sponges and their microbiomes are ecosystem engineers distributed across the globe. However, most research has focused on tropical and temperate sponges, while polar regions like Antarctica have been largely neglected. Despite its harsh conditions and geographical isolation, Antarctica is densely populated by sponges. In this study, we explored the extent of habitat specificity in the diversity, community composition, and microbial co-occurrence within Antarctic sponge microbiomes, in comparison to those from other marine environments. We used massive sequencing of 16S rRNA genes and integrated multiple databases to incorporate Antarctic sponges as a habitat in global microbiome analyses.ResultsOur study revealed significant differences in microbial diversity and community composition between Antarctic and non-Antarctic sponges. We found that most microorganisms present in Antarctic sponges are unique to the South Shetland Islands. Nitrosomonas oligotropha, Candidatus Nitrosopumilus, Polaribacter, SAR116 clade, and Low Salinity Nitrite-Oxidizing Bacteria (LS-NOB) are microbial members characterizing the Antarctic sponge microbiomes. Based on their exclusivity and presence across different sponges worldwide, we identified habitat-specific and habitat-generalist bacteria associated with each habitat. They are particularly abundant and connected within all the Antarctic sponges, suggesting that they may play a crucial role as keystone species within these sponge ecosystems.ConclusionsThis study provides significant insights into the microbial diversity and community composition of sponges in Antarctica and non-Antarctic ecoregions. Our findings provide evidence for habitat-specific patterns that differentiate the microbiomes of Antarctic sponges from elsewhere, indicating the strong influence of environmental selection and dispersal limitation wrapped into the Antarctic ecoregions to shape more similar microbial communities in distantly related sponges. This study contributes to understanding signatures of microbial community assembly in the Antarctic sponges and has important implications for the ecology and evolution of these unique marine environments.

Dataset Information

The Relationship Between Microbiomes and Selective Regimes in the Sponge Genus Ircinia.

Publications

The Relationship Between Microbiomes and Selective Regimes in the Sponge Genus <i>Ircinia</i>.

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