Proteomics Links the Redox State to Calcium Signaling During Bleaching of the Scleractinian Coral Acropora microphthalma on Exposure to High Solar Irradiance and Thermal Stress

Abstract

Shipboard experiments were each performed over a 2 day period to examine the proteomic response of the symbiotic coral Acropora microphthalma exposed to acute conditions of high temperature/low light or high light/low temperature stress. During these treatments, corals had noticeably bleached. The photosynthetic performance of residual algal endosymbionts was severely impaired but showed signs of recovery in both treatments by the end of the second day. Changes in the coral proteome were determined daily and, using recently available annotated genome sequences, the individual contributions of the coral host and algal endosymbionts could be extracted from these data. Quantitative changes in proteins relevant to redox state and calcium metabolism are presented. Notably, expression of common antioxidant proteins was not detected from the coral host but present in the algal endosymbiont proteome. Possible roles for elevated carbonic anhydrase in the coral host are considered: to restore intracellular pH diminished by loss of photosynthetic activity, to indirectly limit intracellular calcium influx linked with enhanced calmodulin expression to impede late-stage symbiont exocytosis, or to enhance inorganic carbon transport to improve the photosynthetic performance of algal symbionts that remain in hospite. Protein effectors of calcium-dependent exocytosis were present in both symbiotic partners. No caspase-family proteins associated with host cell apoptosis, with exception of the autophagy chaperone HSP70, were detected, suggesting that algal loss and photosynthetic dysfunction under these experimental conditions were not due to host-mediated phytosymbiont destruction. Instead, bleaching occurred by symbiont exocytosis and loss of light-harvesting pigments of algae that remain in hospite. These proteomic data are, therefore, consistent with our premise that coral endosymbionts can mediate their own retention or departure from the coral host, which may manifest as “symbiont shuffling” of Symbiodinium clades in response to environmental stress.

Warm-preconditioning protects against acute heat-induced respiratory dysfunction and delays bleaching in a symbiotic sea anemone

“…Our data present an incomplete picture of holobiont metabolism, and application of histological analyses (Dunn et al, 2012) and 'omics' techniques at the post-translational level (Drake et al, 2013;Hillyer et al, 2015;Oakley et al, 2015;Weston et al, 2015), respectively, is needed to confirm or refute the hypothesised changes in aerobic metabolic pathways and mitochondrial densities. Notwithstanding these limitations, this investigation provides some of the first evidence for significant effects of thermal preconditioning on the heat sensitivity of symbiotic cnidarian and Symbiodinium mitochondrial activity.…”

The past, present, and future of coral heat stress studies

“…In particular, combined transcriptome-proteome approaches have the capacity for complementing one another (Seliger et al, 2009), allowing for data integration to provide a better understanding of a system or its current situation (Gomez-Cabrero et al, 2014). A narrow assortment of papers utilizes proteomic analysis to elaborate on fundamental coral biology such as symbiosis, larval development, and calcification (Barneah et al, 2006;Drake et al, 2013;Oakley et al, 2016;Ramos-Silva et al, 2013), but work related to proteomic stress response in corals is sparse Matthews et al, 2017;Weston et al, 2015). While technology and analytical tools are quickly progressing, large-scale studies on proteins are not as feasible as for nucleic acids (Graves & Haystead, 2002).…”

Expression patterns of sterol transporters NPC1 and NPC2 in the cnidarian-dinoflagellate symbiosis

“…Furthermore, only the duplicated copy Avnpc2‐d was upregulated by the symbiotic state, whereas several other symbiosis‐related genes with multiple paralogs were also upregulated in symbiosis. These included genes implicated in host–symbiont recognition, such as C‐type lectins (Grasso et al, ; Rodriguez‐Lanetty, Harii, & Hoegh‐Guldberg, ; Sunagawa et al, ) and Sym32 (Ganot et al, ; Moya, Ganot, Furla, & Sabourault, ; Reynolds, Schwarz, & Weis, ) and genes involved in trafficking and metabolic exchange, such as carbonic anhydrase (Weis & Reynolds, ; Weston et al, ) and Rhbg solute transporters (Ganot et al, ; Sabourault, Ganot, Deleury, Allemand, & Furla, ). In the pea aphid‐bacterial symbiosis, gene duplication plays a role in recruiting amino acid transporters to operate at the symbiotic interface (Duncan et al, ), whereas in Drosophila melanogaster , multiple duplication of npc2 genes has led to differential tissue‐specific expression, with a putative role in binding bacterial cell‐wall components such as peptidoglycans (Shi, Zhong, & Yu, ).…”