Authors: Joseph B. Kelly, David E. Carlson, Jun Siong Low, Robert W. Thacker
Published: 2022-10-04
DOI: 10.1186/s40168-022-01359-z
Source: Full article
AbstractBackgroundTropical members of the sponge genusIrciniapossess highly complex microbiomes that perform a broad spectrum of chemical processes that influence host fitness. Despite the pervasive role of microbiomes inIrciniabiology, 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 11Irciniaspecies 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.ResultsA total of 424 new, high-quality bacterial metagenome-assembled genomes (MAGs) were produced for 10 CaribbeanIrciniaspecies, which were evaluated alongside 113 publicly available MAGs sourced from the Pacific speciesIrcinia 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 ofIrciniametagenomes.ConclusionsThese 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 inIrcinia-associated bacteria is widespread and that these molecules are important for the survival of bacteria in highly complexIrciniamicrobiomes.