Novel trends of genome evolution in highly complex tropical sponge microbiomes.

BACKGROUND: Tropical members of the sponge genus Ircinia possess highly complex microbiomes that perform a broad spectrum of chemical processes that influence host fitness. Despite the pervasive role of microbiomes in Ircinia biology, it is still unknown how they remain in stable association across tropical species. To address this question, we performed a comparative analysis of the microbiomes of 11 Ircinia species using whole-metagenomic shotgun sequencing data to investigate three aspects of bacterial symbiont genomes-the redundancy in metabolic pathways across taxa, the evolution of genes involved in pathogenesis, and the nature of selection acting on genes relevant to secondary metabolism. RESULTS: A total of 424 new, high-quality bacterial metagenome-assembled genomes (MAGs) were produced for 10 Caribbean Ircinia species, which were evaluated alongside 113 publicly available MAGs sourced from the Pacific species Ircinia ramosa. Evidence of redundancy was discovered in that the core genes of several primary metabolic pathways could be found in the genomes of multiple bacterial taxa. Across hosts, the metagenomes were depleted in genes relevant to pathogenicity and enriched in eukaryotic-like proteins (ELPs) that likely mimic the hosts' molecular patterning. Finally, clusters of steroid biosynthesis genes (CSGs), which appear to be under purifying selection and undergo horizontal gene transfer, were found to be a defining feature of Ircinia metagenomes. CONCLUSIONS: These results illustrate patterns of genome evolution within highly complex microbiomes that illuminate how associations with hosts are maintained. The metabolic redundancy within the microbiomes could help buffer the hosts from changes in the ambient chemical and physical regimes and from fluctuations in the population sizes of the individual microbial strains that make up the microbiome. Additionally, the enrichment of ELPs and depletion of LPS and cellular motility genes provide a model for how alternative strategies to virulence can evolve in microbiomes undergoing mixed-mode transmission that do not ultimately result in higher levels of damage (i.e., pathogenicity) to the host. Our last set of results provides evidence that sterol biosynthesis in Ircinia-associated bacteria is widespread and that these molecules are important for the survival of bacteria in highly complex Ircinia microbiomes. Video Abstract.

Context-dependent costs and benefits of endosymbiotic interactions in a ciliate-algae system.

Endosymbiosis, an interaction between two species where one lives within the other, has evolved multiple times independently, but the underlying mechanisms remain unclear. Evolutionary theory suggests that for an endosymbiotic interaction to remain stable over time, births of both partners should be higher than their deaths in symbiosis and deaths of both partners should be higher than their births when living independently. However, experimentally measuring this can be difficult and conclusions tend to focus on the host. Using a ciliate-algal system (Paramecium bursaria host and Chlorella endosymbionts), we estimated the benefits and costs of endosymbiosis for both organisms using fitness measurements in different biotic environments to test under which environmental conditions the net effects of the interaction were positive for both partners. We found that the net effects of harbouring endosymbionts were positive for the ciliate hosts as it allowed them to survive in conditions of low-quality bacteria food. The algae benefitted by being endosymbiotic when predators such as the hosts were present, but the net effects were dependent on the total density of hosts, decreasing as hosts densities increased. Overall, we show that including context-dependency of endosymbiosis is essential in understanding how these interactions have evolved.

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

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.

New shallow water species of Caribbean Ircinia Nardo, 1833 (Porifera: Irciniidae).

Seven Ircinia morphospecies were collected from three sites in the Caribbean (Bocas del Toro, Panama; the Mesoamerican Barrier Reef, Belize; and the Florida Keys, United States of America). Previous research used an integrative taxonomic framework (genome-wide SNP sampling and microbiome profiling) to delimit species boundaries among these Ircinia. Here, we present morphological descriptions for these species, six of which are new to science (Ircinia lowi sp. nov., Ircinia bocatorensis sp. nov., Ircinia radix sp. nov., Ircinia laeviconulosa sp. nov., Ircinia vansoesti sp. nov., Ircinia ruetzleri sp. nov.) in addition to one species conferre (Ircinia cf. reteplana Topsent, 1923).

Tissue-resident memory T cell reactivation by diverse antigen-presenting cells imparts distinct functional responses.

CD8+ tissue-resident memory T cells (TRM cells) are poised at the portals of infection and provide long-term protective immunity. Despite their critical roles, the precise mechanics governing TRM cell reactivation in situ are unknown. Using a TCR-transgenic Nur77-GFP reporter to distinguish "antigen-specific" from "bystander" reactivation, we demonstrate that lung CD8+ TRM cells are reactivated more quickly, yet less efficiently, than their counterparts in the draining LNs (TLN cells). Global profiling of reactivated memory T cells revealed tissue-defined and temporally regulated recall response programs. Unlike the reactivation of CD8+ TLN cells, which is strictly dependent on CD11c+XCR1+ APCs, numerous antigen-presenting partners, both hematopoietic and non-hematopoietic, were sufficient to reactivate lung CD8+ TRM cells, but the quality of TRM cell functional responses depended on the identity of the APCs. Together, this work uncovers fundamental differences in the activation kinetics, mechanics, and effector responses between CD8+ memory T cells in peripheral vs. lymphoid organs, revealing a novel tissue-specific paradigm for the reactivation of memory CD8+ T cells.