Restructuring of the sponge microbiome favors tolerance to ocean acidification

Abstract

Ocean acidification is increasing and affects many marine organisms. However, certain sponge species can withstand low-pH conditions. This may be related to their complex association with microbes. We hypothesized that species with greater microbial diversity may develop functional redundancy that could enable the holobiont to survive even if particular microbes are lost at low-pH conditions. We evaluated the effects of acidification on the growth and associated microbes of three ubiquitous Mediterranean sponges by exposing them to the present pH level and that predicted for the year 2100. We found marked differences among the species in the acquisition of new microbes, being high in Dysidea avara, moderate in Agelas oroides and null in Chondrosia reniformis; however, we did not observe variation in the overall microbiome abundance, richness or diversity. The relative abilities to alter the microbiomes contributes to survivorship in an OA scenario as demonstrated by lowered pH severely affecting the growth of C. reniformis, halving that of A. oroides, and unaffecting D. avara. Our results indicate that functional stability of the sponge holobiont to withstand future OA is species-specific and is linked to the species' ability to use horizontal transmission to modify the associated microbiome to adapt to environmental change.

Phylogeny and genomics of SAUL, an enigmatic bacterial lineage frequently associated with marine sponges

“…Sponge symbionts exhibit resistance mechanisms designed to specifically address changes in host conditions that generally lead to stress. In this context, genomic studies of sponge‐associated microbial communities have revealed an enrichment of stress‐related proteins (López‐Legentil et al ., ; Fan et al ., ; Liu et al ., ) that may help symbionts cope with environmental stressors, including the presence of antimicrobial compounds (Piel, ), bioaccumulation of heavy metals (Hansen et al ., ; Webster et al ., ), and changes in temperature (Fan et al ., ), pH (Ribes et al ., ) and sedimentation (Luter et al ., ). The SAUL clade possesses genomic signatures related to adaptation to the microenvironment of the host sponge, with both bins carrying genes encoding proteins such as UspA (universal stress protein A) (annotated as COG0589), which is synthesised in response to environmental stress such as heat and/or osmotic shock, nutrient starvation, or exposure to heavy metals (Nyström and Neidhardt, ; Kvint et al ., ).…”

Dissolved inorganic nitrogen fluxes from common Florida Bay (U.S.A.) sponges

“…During our chamber experiments, pH was not measured and any impacts of lowered pH on the tested sponge holobionts remain unknown. However, previous work indicated that the microbiome of Mediterranean sponges was relatively stable in terms of abundance, richness, and diversity under comparable pH shifts (> 60 d at a pH ≈ 7.8; Ribes et al ). The impact of this pH shift on the metabolic function of the microbiome is unknown, but we posit the brevity of the exposure to a large magnitude shift will temper any impact.…”

Marine Animal Microbiomes: Toward Understanding Host–Microbiome Interactions in a Changing Ocean

“…Most recently, microbial symbionts of tropical sponges were shown to produce and store polyphosphate granules (Zhang et al, 2015), perhaps enabling the host to survive periods of phosphate depletion in oligotrophic marine environments (Colman, 2015). The microbiomes of some sponge species do appear to change in community structure in response to changing environmental conditions, including temperature (Simister et al, 2012a) and ocean acidification (Morrow et al, 2015;Ribes et al, 2016), as well as synergistic impacts (Lesser et al, 2016). Understanding the effect of these altered host-microbiome interactions on sponge growth and ecology are topics for further research.…”