The response of a boreal deep-sea sponge holobiont to acute thermal stress

Abstract

Effects of elevated seawater temperatures on deep-water benthos has been poorly studied, despite reports of increased seawater temperature (up to 4 °C over 24 hrs) coinciding with mass mortality events of the sponge Geodia barretti at Tisler Reef, Norway. While the mechanisms driving these mortality events are unclear, manipulative laboratory experiments were conducted to quantify the effects of elevated temperature (up to 5 °C, above ambient levels) on the ecophysiology (respiration rate, nutrient uptake, cellular integrity and sponge microbiome) of G. barretti. No visible signs of stress (tissue necrosis or discolouration) were evident across experimental treatments; however, significant interactive effects of time and treatment on respiration, nutrient production and cellular stress were detected. Respiration rates and nitrogen effluxes doubled in responses to elevated temperatures (11 °C & 12 °C) compared to control temperatures (7 °C). Cellular stress, as measured through lysosomal destabilisation, was 2–5 times higher at elevated temperatures than for control temperatures. However, the microbiome of G. barretti remained stable throughout the experiment, irrespective of temperature treatment. Mortality was not evident and respiration rates returned to pre-experimental levels during recovery. These results suggest other environmental processes, either alone or in combination with elevated temperature, contributed to the mortality of G. barretti at Tisler reef.

Elevated seawater temperature disrupts the microbiome of an ecologically important bioeroding sponge

“…In many sponge species, microbial shifts at high temperatures coincide with declining host health (Fan et al., ; Lemoine et al., ; López‐Legentil et al., ; Luter et al., ; Simister, Taylor et al., ; Webster et al., ), whereas other sponges are able to maintain stable microbial communities irrespective of seawater temperature (Lesser, Fiore, Slattery, & Zaneveld, ; Pita, Erwin, Turon, & López‐Legentil, ; Strand et al., ; Webster, Botté et al., ). Microbial shifts can lead to dysbiosis, including reduced expression of genes related to nutrient transport, substrate utilization, sugar metabolism and cellular integrity in the symbionts and increased expression of stress response genes in the sponge (Fan et al., ).…”

“…The sponge microbiome can also shift upon exposure to elevated temperature (Lemoine, Buell, Hill, & Hill, ; López‐Legentil, Song, McMurray, & Pawlik, ; Webster et al., ). However, some sponge species are able to maintain stable communities regardless of temperature (Strand et al., ; Webster, Botté, Soo, & Whalan, ), while others retain their symbionts until the very late stages of heat stress when the sponge itself exhibits necrosis (Luter, Whalan, & Webster, ; Simister, Taylor et al., ; Webster et al., ). Little is known about the microbial communities of bioeroding sponges and, in particular, the sensitivity of the microbiome to elevated sea surface temperatures.…”

Distribution of Deep-Sea Sponge Aggregations in an Area of Multisectoral Activities and Changing Oceanic Conditions

“…These variables include water temperature, salinity and silicate concentrations Knudby et al, 2013;Beazley et al, 2015;Howell et al, 2016), topography, internal waves, current speeds, food supply (Rice et al, 1990;Klitgaard and Tendal, 2004;Knudby et al, 2013;Howell et al, 2016). Establishing a precise relationship between the contribution of each of the environmental parameters mentioned above and the distribution of deep-sea sponges/deepsea sponge aggregations is still an open question given the limited availability of data on (a) species' physiological tolerances, (b) geographical/bathymetric distribution of these organisms and (c) measurements of environmental data at appropriate spatial scales (Tjensvoll et al, 2013;Beazley et al, 2015;Strand et al, 2017). In the present study, the values of temperature per transect inside the FSC NCMPA ranged from 6.5 • C (transect F) to ∼8.9 • C (transect D) and salinity values ranged from 34.9 psu (transect D) to 35.1 psu (transect C; Table 1); these values fall within the temperature and salinity range reported up to now for Geodia sponges in the North East Atlantic (Klitgaard and Tendal, 2004;Bett, 2012).…”

Thermal stress modifies the marine sponge virome

“…In this context, a considerable body of research has explored how sponge hosts and their associated microbial communities respond to ocean warming (Lemoine et al ., ; López‐Legentil et al ., ; Webster et al ., ; Lopez‐Legentil et al ., ; Webster et al ., ; Fan et al ., ; Simister et al ., ; Pita et al ., ). Overall, responses are highly species‐specific (Bennett et al ., ; Bennett et al ., ), with some studies showing shifts in the microbiome under thermal stress (López‐Legentil et al ., ) and others demonstrating remarkably stable microbial communities irrespective of temperature and/or host health state (Simister et al ., ; Strand et al ., ). In contrast, the response of sponge‐associated viral communities to thermal stress has never been assessed.…”