A genomic view of the microbiome of coral reef demosponges

Abstract

Sponges underpin the productivity of coral reefs, yet few of their microbial symbionts have been functionally characterised. Here we present an analysis of ~1200 metagenome-assembled genomes (MAGs) spanning seven sponge species and 25 microbial phyla. Compared to MAGs derived from reef seawater, sponge-associated MAGs were enriched in glycosyl hydrolases targeting components of sponge tissue, coral mucus and macroalgae, revealing a critical role for sponge symbionts in cycling reef organic matter. Further, visualisation of the distribution of these genes amongst symbiont taxa uncovered functional guilds for reef organic matter degradation. Genes for the utilisation of sialic acids and glycosaminoglycans present in sponge tissue were found in specific microbial lineages that also encoded genes for attachment to sponge-derived fibronectins and cadherins, suggesting these lineages can utilise specific structural elements of sponge tissue. Further, genes encoding CRISPR and restriction-modification systems used in defence against mobile genetic elements were enriched in sponge symbionts, along with eukaryote-like gene motifs thought to be involved in maintaining host association. Finally, we provide evidence that many of these sponge-enriched genes are laterally transferred between microbial taxa, suggesting they confer a selective advantage within the sponge niche and therefore play a critical role in host ecology and evolution.

Genomes of Novel Myxococcota Reveal Severely Curtailed Machineries for Predation and Cellular Differentiation

“…Further, multiple ampliconbased diversity surveys have identified Myxococcota-affiliated sequences in non-soil habitats, many of which represent anoxic/ hypoxic settings (18)(19)(20)(21)(22)(23)(24). Recently, the implementation of genome-resolved metagenomic approaches has resulted in the recovery of Myxococcota genomes from a wide range of non-soil habitats, almost invariably constituting a minor fraction of the population (25)(26)(27)(28)(29)(30). Interestingly, many of these yet-uncultured lineages identified using 16S rRNA gene amplicon or metagenomic surveys appear to represent distinct novel, yetuncultured lineages within the Myxococcota.…”

Sponge–Microbe Interactions on Coral Reefs: Multiple Evolutionary Solutions to a Complex Environment

“…For example, genes and transcripts involved in methylotrophy and other C 1 metabolism were observed in several high throughputsequencing based studies of sponge symbionts (Thomas et al, 2010;Fan et al, 2012;Radax et al, 2012;Li et al, 2014;Moitinho-Silva et al, 2014;Fiore et al, 2015a). Additionally, recent metagenomic analysis of six sponge microbiomes of the class Demospongiae supports the presence of functional guilds that target DOM like sialic acids derived from sponge tissue and carbohydrates derived from coral and algal DOM (Robbins et al, 2021). Symbiont-specific examples include the ability to consume diverse carbon sources including chitin, cellulose, and/or N-acetylglucosamine by Entotheonella (Liu et al, 2016) and Poribacteria (Siegl et al, 2011), and steroids by Actinobacteria, Alphaproteobacteria, and Gammaproteobacteria in sponges (Holert et al, 2018).…”

“…However, we argue that the corresponding results should be placed in the context of the broader and more complicated picture of sponge holobiont ecology rather than viewed in isolation as a single factor (e.g., top-down vs. bottom-up processes). Furthermore, the field of sponge ecology should weave together the individually discovered narratives on molecular and genomic functional attributes of sponges and/or microbial symbionts (e.g., Letourneau et al, 2020;Robbins et al, 2021), underlying evolutionary patterns (e.g., Freeman et al, 2020;Kelly et al, 2021), and ecological interactions (e.g., Loh and Pawlik, 2014;Pawlik et al, 2018;Wulff, 2020), to better develop a framework for understanding ecological and molecular mechanisms relevant to the success of extant poriferans. This work is likely to have implications beyond the field of sponge biology.…”

The Chloroflexi supergroup is metabolically diverse and representatives have novel genes for non-photosynthesis based CO2 fixation

“…The ability to reconstruct draft genomes from metagenomes circumvents the cultivation requirement and has greatly expanded the genomic coverage of the Chloroflexota and related bacteria. Two distinct groups represented by genomes from metagenomes are the ANG-CHLX, first reported from soil in northern California [4] and now renamed as Dormibacteraeota [5] , and RIF-CHLX, first reported from an aquifer adjacent to the Colorado River near the town of Rifle, CO [6] [34] and later designated as Chloroflexota class ca. Limnocylindria [7] .…”