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. 2017 May 22;7(1):1660.
doi: 10.1038/s41598-017-01091-x.

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

R Strand  1   2 , S Whalan  3 , N S Webster  4   5 , T Kutti  1 , J K H Fang  1 , H M Luter  4   6 , R J Bannister  7
Affiliations

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

R Strand et al. Sci Rep. .

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.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1
Left panel–Mean respiration rate (μmol O2 g (tissue DW)−1 h−1) ± S.E. (n = 5) of cultivated G. barretti explants exposed to four different temperature levels (7 °C–Black bar, 9 °C–Dark grey bar, 11 °C–Light grey bar & 12 °C–White bar) over a 14 d experimental period. R on the x-axis is respiration at 65 d post exposure (the recovery period), with explants being maintained at ambient temperatures (7 °C) after the 14 d experimental period, irrespective of prior temperature exposure. Right panel–Interaction plot of estimated marginal means of respiration rates calculated for each temperature (7 °C–Black circles, 9 °C–Dark grey triangles, 11 °C–Light grey squares & 12 °C–White diamonds) at each exposure day and recovery time period (R).
Figure 2
Figure 2
Left panel–Mean net nitrogen efflux rate (μmol NO2 − + NO3 − g(tissue DW)−1 h−1) ± S.E. (n = 5) by G. barretti explants exposed to four different temperature levels (7 °C–Black bar, 9 °C–Dark grey bar, 11 °C–Light grey bar & 12 °C–White bar) over a 14 d experimental period. R on the x-axis is respiration at 65 d post exposure (the recovery period), with explants being maintained at ambient temperatures (7 °C) after the 14 d experimental period, irrespective of prior temperature exposure. Right panel–Interaction plot of estimated marginal means of nitrogen (NO2 − + NO3 −) flux rates calculated for each temperature (7 °C–Black circles, 9 °C–Dark grey triangles, 11 °C–Light grey squares & 12 °C–White diamonds) at each exposure day and recovery time period (R).
Figure 3
Figure 3
Left panel–Mean net phosphate efflux rate (μmol PO4 3− g(tissue DW)−1 h−1) ± 1 S.E. (n = 5) by G. barretti explants exposed to four different temperature levels (7 °C–Black bar, 9 °C–Dark grey bar, 11 °C–Light grey bar & 12 °C–White bar) over a 14 d experimental period. R on the x-axis is respiration at 65 d post exposure (the recovery period), with explants being maintained at ambient temperatures (7 °C) after the 14 d experimental period, irrespective of prior temperature exposure. Right panel–Interaction plot of estimated marginal means of PO4 3− flux rates calculated for each temperature (7 °C–Black circles, 9 °C–Dark grey triangles, 11 °C–Light grey squares & 12 °C–White diamonds) at each exposure day and recovery time period (R).
Figure 4
Figure 4
Mean net silicate uptake rate (μmol SiO4 4− g(tissue DW)−1 h−1) ± S.E. (n = 5) by G. barretti explants exposed to four different temperature levels (7 °C–Black bar, 9 °C–Dark grey bar, 11 °C–Light grey bar & 12 °C–White bar) over a 14 d experimental period. R on the x-axis is respiration at 65 d post exposure (the recovery period), with explants being maintained at ambient temperatures (7 °C) after the 14 d experimental period, irrespective of prior temperature exposure.
Figure 5
Figure 5
Left panel–Mean percentages (%) of cells with destabilised lysosomal membranes ± S.E. (n = 5) of G. barretti explants exposed to four different temperature levels (7 °C–Black bar, 9 °C–Dark grey bar, 11 °C–Light grey bar & 12 °C–White bar) over a 14 d experimental period. R on the x-axis is respiration at 65 d post exposure (the recovery period), with explants being maintained at ambient temperatures (7 °C) after the 14 d experimental period, irrespective of prior temperature exposure. Right panel–Interaction plot of estimated marginal means of lysosomal membrane destabilisation calculated for each temperature (7 °C–Black circles, 9 °C–Dark grey triangles, 11 °C–Light grey squares & 12 °C–White diamonds) at each exposure day and recovery time period (R).
Figure 6
Figure 6
Principal coordinate analysis (PCO) of the bacterial OTUs from G. barretti explants exposed to four different temperature levels (see attached legend) over a 14 d experimental period. R on the legend represents 65 d post exposure (the recovery period), with explants being maintained at ambient temperatures (7 °C) after the 14 d experimental period, irrespective of prior temperature exposure.
See this image and copyright information in PMC

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