Host-microbe Interactions

Today we look at animals as 'holobionts'. These comprise the eukaryotic host and microorganisms that are tightly associated to it. In fact it is now well accepted that animals exist only in partnership with symbionts that affect the health of such multi-organismal entities. Our laboratory investigates the interactions within holobionts using as model system marine sponges.

With sponges possibly being the earliest branching extant animal lineage, sponges are ideally evolutionary placed to inform our understanding of the early evolution of host-microbe symbioses. 

We look at the molecular mechanisms involved in the establishment and maintenance of the interaction of the sponge with its microbial symbionts. One aspect is to determine how components of what could be considered an ancient innate immune system (of the sponge) may serve the sponge to differentiate between microbial symbionts and microbial food (or pathogens). Using substractive hybridization techniques we identified a sponge-gene containing a scavenger receptor cystein rich (SRCR) domain that was differentially expressed in the presence versus absence of cyanobacterial symbionts (Steindler et al, Mar Biotechnol 2007). Proteins featuring SRCR domains are either cell surface or secreted proteins and in vertebrates have functions related to host-defense during endocytosis. We hypothesized that sponge genes with SRCR domain that are differentially expressed in relation to presence/absence of microbial symbionts may have a function in the recognition of the symbiont.

Presently we are utilizing transcriptomic-based approaches to gain a more global overview of the genes that are differentially expressed in the sponge in function of the symbiotic state with cyanobacterial symbionts. Further, we seek for mechanisms of host-symbiont recognition also within the genomes of sponge symbionts. The latter are sequenced by next-generation sequencing, assembled by bioinformatic-binning methods, and then compared to available genomes of the phylogenetically clo sest free-living bacteria.

Methane Cycling In Sponge Holobionts

Ocean surface waters are natural sources of methane emission to the atmosphere, in particular at coastal areas. Given the properties of methane as a greenhouse gas, characterizing novel sources and sinks of methane is crucial for the prediction of climate responses and biogeochemical feedbacks. Methane cycling potential has not been assessed in the microbiota hosted by marine invertebrates, except for those growing at methane seeps, where methane sources are abiotic. However, biotic sources for methane may also be present in host-associated system, such as marine sponges, which contain 2-4 orders of magnitude higher bacterial cell densities than the surrounding seawater. The potential for biotic methane production by sponge symbionts is supported by recent findings of methane-consuming bacteria, even in sponges growing far from abiotic methane sources. Using both public metagenomic and novel sponge metatranscriptomic datasets we found genetic potential for aerobic methane synthesis via transformation of dissolved organic nutrients in sponge symbionts. We therefore hypothesize that sponges, through their associated microbiota, are a significant source of methane in the global ocean, that has not previously been accounted for in models of ocean methane cycling. For more information please visit the following links below https://tinyurl.com/ms8wfw6s  and  https://youtu.be/cRxlXrbM_qo 

Sponges And Biotechnology

Sponges are also a major reservoir of natural diversity, with an incredible range of different bacterial phyla that are potential source of new enzymes and small molecules of interest for the chemical industry and medicine. We use novel high-throughput microbial cultivation methods to try and cultivate such majority of yet-uncultured sponge symbionts. Furthermore, we use cosmid library screenings, and bioinformatic analysis on metagenomics data derived from sponge microbiomes to search for genes responsible for the production of secondary metabolites of interest. 


Graphical abstract from Cerrano, C., Giovine, M., & Steindler, L. (2022). Petrosia ficiformis (Poiret, 1789): An excellent model for holobiont and biotechnological studies. Current Opinion in Biotechnology, 74, 61-65. The graph was designed by Cláudia Ferreira.