Broad scale proteomic analysis of heat-destabilised symbiosis in the hard coral Acropora millepora

Abstract

Coral reefs across the globe are threatened by warming oceans. The last few years have seen the worst mass coral bleaching events recorded, with more than one quarter of all reefs irreversibly impacted. Considering the widespread devastation, we need to increase our efforts to understanding the physiological and metabolic shifts underlying the breakdown of this important symbiotic ecosystem. Here, we investigated the proteome (PRIDE accession # PXD011668) of both host and symbionts of the reef-building coral Acropora millepora exposed to ambient (~ 28 °C) and elevated temperature (~ 32 °C for 2 days, following a five-day incremental increase) and explored associated biomolecular changes in the symbiont, with the aim of gaining new insights into the mechanisms underpinning the collapse of the coral symbiosis. We identified 1,230 unique proteins (774 host and 456 symbiont) in the control and thermally stressed corals, of which 107 significantly increased and 125 decreased in abundance under elevated temperature relative to the control. Proteins involved in oxidative stress and proteolysis constituted 29% of the host proteins that increased in abundance, with evidence of impairment to endoplasmic reticulum and cytoskeletal regulation proteins. In the symbiont, we detected a decrease in proteins responsible for photosynthesis and energy production (33% of proteins decreased in abundance), yet minimal signs of oxidative stress or proteolysis. Lipid stores increased > twofold despite reduction in photosynthesis, suggesting reduced translocation of carbon to the host. There were significant changes in proteins related to symbiotic state, including proteins linked to nitrogen metabolism in the host and the V-ATPase (-0.6 fold change) known to control symbiosome acidity. These results highlight key differences in host and symbiont proteomic adjustments under elevated temperature and identify two key proteins directly involved in bilateral nutrient exchange as potential indicators of symbiosis breakdown.

Shotgun Proteomics Identifies Active Metabolic Pathways in Bleached Coral Tissue and Intraskeletal Compartments

“…Several enzymes involved in oxidative stress response were at higher abundance in both the OL and IC of bleached M. capitata compared to samples from non-bleached corals. This observation is consistent with proteomics (e.g., Weston et al, 2015;Cziesielski et al, 2018;Petrou et al, 2021) and transcriptomics (e.g., DeSalvo et al, 2008DeSalvo et al, , 2010Voolstra et al, 2009) studies that have demonstrated increased antioxidant activity in response to thermal stress in cnidarians. Multiple catalases (CAT) were elevated in the OL and IC of bleached corals.…”

“…Proteomics has proven to be a valuable tool for uncovering active cellular processes and elucidating the response of different biological compartments of symbiotic cnidarians in response to stress (Weston et al, 2015;Ricaurte et al, 2016;Cziesielski et al, 2018;Hernández-Elizárraga et al, 2019;Mayfield, 2020;Mayfield et al, 2021;Petrou et al, 2021). Our high-throughput discovery-based proteomic analyses of the OL and IC of bleached and non-bleached corals support our hypothesis that proteomic signatures differ between M. capitata OL and IC, reflecting different biological functions associated with these two compartments.…”

“…Malate synthetase (MS), the other key enzyme of the glyoxylate cycle that converts glyoxylate and acetyl-CoA to malate, was present in the proteomes identified in this study, but no significant difference was detected between bleached and non-bleached corals. The same trend of increased ISL abundance and no increase in MS abundance has been reported for Porites asteroides (Kenkel et al, 2013) and Acropora millepora (Petrou et al, 2021). We also detected three key enzymes involved in lipid metabolism in higher abundance in the OL of bleached corals compared to the OL of non-bleached corals: very long-chain specific acyl-CoA dehydrogenase (ACADVL), medium chain specific acyl-CoA dehydrogenase (ACADM) and acetyl-CoA acetyltransferase (ACAT1).…”

“…Although it was once thought to only occur in plants and bacteria, recent transcriptomics studies have shown that glyoxylate cycle enzymes also occur in corals (DeSalvo et al, 2010;Kenkel et al, 2013;Polato et al, 2013). Bleached corals may upregulate the glyoxylate cycle, or the production of glyoxylate, to metabolize energy in stored lipids, breaking down triacylglycerol into their component fatty acids for release of acetyl-CoA, when carbohydrate supply is low (Polato et al, 2013;Wright et al, 2015;Petrou et al, 2021). Malate synthetase (MS), the other key enzyme of the glyoxylate cycle that converts glyoxylate and acetyl-CoA to malate, was present in the proteomes identified in this study, but no significant difference was detected between bleached and non-bleached corals.…”

Multi-Omics Revealing the Response Patterns of Symbiotic Microorganisms and Host Metabolism in Scleractinian Coral Pavona minuta to Temperature Stresses

“…As the main consequence of climate change, ocean warming is seriously threatening the survival of coral reefs [3]. Many studies have been conducted to explore the response patterns of corals to the elevated temperature by diverse methods [4][5][6]. For example, divergent responses to heat stress by different coral taxa has been found in the Great Barrier Reef, resulting in the regional-scale shift in the composition of coral assemblages [7].…”