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. 2023 Nov 25;13(1):20724.
doi: 10.1038/s41598-023-48020-9.

Symbiodiniaceae photophysiology and stress resilience is enhanced by microbial associations

Jennifer L Matthews #  1 , Lilian Hoch #  2 , Jean-Baptiste Raina  2 , Marine Pablo  2   3 , David J Hughes  2   4 , Emma F Camp  2 , Justin R Seymour  2 , Peter J Ralph  2 , David J Suggett  2   5 , Andrei Herdean  2
Affiliations

Symbiodiniaceae photophysiology and stress resilience is enhanced by microbial associations

Jennifer L Matthews et al. Sci Rep. .

Abstract

Symbiodiniaceae form associations with extra- and intracellular bacterial symbionts, both in culture and in symbiosis with corals. Bacterial associates can regulate Symbiodiniaceae fitness in terms of growth, calcification and photophysiology. However, the influence of these bacteria on interactive stressors, such as temperature and light, which are known to influence Symbiodiniaceae physiology, remains unclear. Here, we examined the photophysiological response of two Symbiodiniaceae species (Symbiodinium microadriaticum and Breviolum minutum) cultured under acute temperature and light stress with specific bacterial partners from their microbiome (Labrenzia (Roseibium) alexandrii, Marinobacter adhaerens or Muricauda aquimarina). Overall, bacterial presence positively impacted Symbiodiniaceae core photosynthetic health (photosystem II [PSII] quantum yield) and photoprotective capacity (non-photochemical quenching; NPQ) compared to cultures with all extracellular bacteria removed, although specific benefits were variable across Symbiodiniaceae genera and growth phase. Symbiodiniaceae co-cultured with M. aquimarina displayed an inverse NPQ response under high temperatures and light, and those with L. alexandrii demonstrated a lowered threshold for induction of NPQ, potentially through the provision of antioxidant compounds such as zeaxanthin (produced by Muricauda spp.) and dimethylsulfoniopropionate (DMSP; produced by this strain of L. alexandrii). Our co-culture approach empirically demonstrates the benefits bacteria can deliver to Symbiodiniaceae photochemical performance, providing evidence that bacterial associates can play important functional roles for Symbiodiniaceae.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
The effect of associated bacteria on the growth of Symbiodinium microadriaticum and Breviolum minutum. The growth of both (A) S. microadriaticum and (B) B. minutum was enhanced by the presence of bacteria compared to extracellular bacteria removed (EBR) cultures. Dotted lines are photophysiological sample time points, pinpointing early- (3 days, black line) and mid-exponential (7 days, grey line) growth phases. Values are natural log of relative chlorophyll intensity (n = 4).
Figure 2
Figure 2
Maximum effective quantum yield (Fv/Fm) of modified Symbiodiniaceae-bacteria associations. Fv/Fm measurements were taken from cultures of S. microadriaticum (A & B) and B. minutum (C & D) that had been either untreated, had all extracellular bacteria removed (EBR), or co-cultured with either L. alexandrii, M. adhaerens or M. aquimarina. Measurements were taken at early (A & C) and mid-exponential growth (B & D) at control temperature (26 °C). Lowercase letters indicate ANOVA post-hoc grouping (n = 5).
Figure 3
Figure 3
ETR surface plots of Symbiodiniaceae-bacteria co-cultures. Symbiodinium microadriaticum (left, A–J) and Breviolum minutum (right, K–T) were incubated without bacteria (EBR, A,F,K,L), or with L. alexandrii (B, G, M, N), M. adhaerens (C, H, O, P), or M. aquimarina (D, I, Q, R), or were left untreated (E, J, S, T). The ETR was measure during early- (A–E, K–S) and mid-exponential (F–J, L–T) growth across temperatures (18–35 °C) and light (0–800 PAR) ranges. Surface plots are scaled to maximum and minimum ETR recorded by the Phenoplate. Grey area indicates readings that exceeded the maximum ETR detection threshold on the Phenoplate. Data available in Table S4.
Figure 4
Figure 4
NPQ surface plots of Symbiodiniaceae-bacteria co-cultures. Symbiodinium microadriaticum (left, A–J) and Breviolum minutum (right, K–T) were incubated without bacteria (EBR, A,F,K,L), or with L. alexandrii (B, G, M, N), M. adhaerens (C, H, O, P), or M. aquimarina (D, I, Q, R), or were left untreated (E, J, S, T). The NPQ was measure during early- (A–E, K–S) and mid-exponential (F–J, L–T) growth across temperatures (18–35 °C) and light (0–800 PAR) ranges. Surface plots are scaled to maximum and minimum NPQ recorded by the Phenoplate. Grey area indicates readings that exceeded the maximum NPQ detection threshold on the Phenoplate. Data available in Table S4.
Figure 5
Figure 5
The maximum photochemical and photoprotective capacity of Symbiodinium microadriaticum-bacteria associations across temperatures. Maximum relative electron transport rate (rETRmax; A & B) and non-photochemical quenching (NPQmax; C & D) at early (A & C) and mid-exponential growth (B & D) were calculated across the temperature range (18–35 °C). Polynomial curves were fitted to the plots to represent general trends. n = 5 per treatment.
Figure 6
Figure 6
The maximum photochemical and photoprotective capacity of Breviolum minutum-bacteria associations across temperatures. Maximum relative electron transport rate (rETRmax; A & B) and non-photochemical quenching (NPQmax; C & D) at early (A & C) and mid-exponential growth (B & D) were calculated across the temperature range (18–35 °C). Polynomial curves were fitted to the plots to represent general trends. n = 5 per treatment.
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