Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress

Abstract

Large-scale mortality of marine invertebrates is a major global concern for ocean ecosystems and many sessile, reef-building animals, such as sponges and corals, are experiencing significant declines through temperature-induced disease and bleaching. The health and survival of marine invertebrates is often dependent on intimate symbiotic associations with complex microbial communities, yet we have a very limited understanding of the detailed biology and ecology of both the host and the symbiont community in response to environmental stressors, such as elevated seawater temperatures. Here, we use the ecologically important sponge Rhopaloeides odorabile as a model to explore the changes in symbiosis during the development of temperature-induced necrosis. Expression profiling of the sponge host was examined in conjunction with the phylogenetic and functional structure and the expression profile of the symbiont community. Elevated temperature causes an immediate stress response in both the host and symbiont community, including reduced expression of functions that mediate their partnership. Disruption to nutritional interdependence and molecular interactions during early heat stress further destabilizes the holobiont, ultimately leading to the loss of archetypal sponge symbionts and the introduction of new microorganisms that have functional and expression profiles consistent with a scavenging lifestyle, a lack virulence functions and a high growth rate. Previous models have postulated various mechanisms of mortality and disease in marine invertebrates. Our study suggests that interruption of symbiotic interactions is a major determinant for mortality in marine sessile invertebrates. High symbiont specialization and low functional redundancy, thus make these holobionts extremely vulnerable to environmental perturbations, including climate change.

Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection

“…Nevertheless, the high abundance of Arcobacter spp. strains in moribund oysters, starved abalones (Tanaka et al, 2004) and necrotic sponges (Fan et al, 2013) may suggest their potential as opportunistic pathogens when occurring in high enough densities (Olson et al, 2014). Dominance of Arcobacter spp.…”

“…Shifts from mutualist-to pathogen-dominated communities due to global warming have already been reported (Ritchie, 2006), as well as an increase in occurrence of infectious diseases (Altizer et al, 2013). At lower latitudes, warming usually implies crossing the upper limits of thermal tolerance and is almost certain to have adverse effects on the affected organisms (Lafferty et al, 2004;Fan et al, 2013). The outcome in temperate regions can be much less predictable, depending on thermal optima and ranges of hosts and pathogens (Thomas and Blanford, 2003).…”

“…However, seasonality does not equal temperature (Farcy et al, 2007;Gilbert et al, 2012) and experimental studies addressing the temperature-dependent short-term microbial dynamics, which may be highly relevant to development of disease, are mostly confined to corals and sponges (Vega Thurber et al, 2009;Simister et al, 2012;Fan et al, 2013).…”

Publication impact in sponge chemical and microbial ecology

“…Additionally, there are number of papers on spatiotemporal dynamics of associated microbial communities assessing bacterial and also archaeal biodiversity (Sacristán-Soriano et al 2011b, Bjork et al 2013, Hardoim and Costa 2014. Some themes are receiving increasing attention from the scientific community due to the importance of the associated microbial community on sponge health, yet little research has focused attention on the resilience of sponge-microbe interactions to a changing climate or anthropogenic disturbances (Bell et al 2013, Fan et al 2013. Changes in environmental conditions might induce a number of sponge diseases if the host-symbiont partnership breaks down or deviates from normal functioning (Webster et al 2008, Angermeier et al 2012.…”

“…We are just starting to understand the importance of microbial symbionts on sponge health. We are yet to make significant progress in topics such as sponge disease and assessing the sensitivity of sponge symbioses (Bell et al 2013, Fan et al 2013) and chemical profiles (Duckworth et al 2012) to environmental stressors such as climate change. A breakdown in host-symbiont partnerships or the alteration of the sponge chemistry as a result of global warming or anthropogenic disturbances may profoundly affect the ability of sponges to protect themselves from predation, fouling, or infections (Webster et al 2008, Angermeier et al 2012).…”