Metabolome shift associated with thermal stress in coral holobionts

Abstract

23Coral reef systems are under global threat due to warming and acidifying oceans 1 . 24Understanding the response of the coral holobiont to environmental change is crucial to aid 25 conservation efforts. The most pressing problem is "coral bleaching", usually precipitated 26 by prolonged thermal stress that disrupts the algal symbiosis sustaining the holobiont 2,3 . We 27 used metabolomics to understand how the coral holobiont metabolome responds to heat 28 stress with the goal of identifying diagnostic markers prior to bleaching onset. We studied 29 the heat tolerant Montipora capitata and heat sensitive Pocillopora acuta coral species from 30 the Hawaiian reef system in Kāne'ohe Bay, O'ahu. Untargeted LC-MS analysis uncovered 31 both known and novel metabolites that accumulate during heat stress. Among those showing 32 the highest differential accumulation were a variety of co-regulated dipeptides present in 33 both species. The structures of four of these compounds were determined (Arginine-34 Glutamine, Lysine-Glutamine, Arginine-Valine, and Arginine-Alanine). These dipeptides 35 also showed differential accumulation in symbiotic and aposymbiotic (alga free) individuals 36 of the sea anemone model Aiptasia 4 , suggesting their animal provenance and algal symbiont 37 related function. Our results identify a suite of metabolites associated with thermal stress 38 that can be used to diagnose coral health in wild samples. 39 40 The exchange of metabolites, either between organism-environment or organism-organism, gave 41 rise not only to early life, but complex life systems on Earth. Examples include bacterial deep vent 42communities 5 , the plant rhizosphere 6 , the human microbiome 7 , and the coral holobiont 8 . Exchange 43 of metabolites between stony corals (Scleractinia), their dinoflagellate algal photosymbionts 44 (Symbiodiniaceae), and associated microbes is the foundation for modern coral reef ecosystems 1,9 45 that cover ca. 255,000 km 2 of the planet surface 10 . Under ambient conditions, the algal cells 46 provide 90-95% of host energy needs in the form of lipids, carbohydrates, amino acids, and O2 11 . 47

Multi-omic characterization of the thermal stress phenome in the stony coralMontipora capitata

“…The second aspect we wish to consider is the impact of thermal stress on the coral reproductive cycle. Beyond the MAGI results regarding progesterone, analysis of existing metabolite ion counts from untargeted UHPLC-MS analysis of M. capitata (11) shows that predicted sex steroids in this species follow the expected increase in accumulation (e.g., testosterone, estrone, androstenedione) under ambient conditions during the mass spawning event ( Figure 5). These metabolite levels are generally reduced under thermal stress, however, at T5, recovery to near ambient and wild sample levels are found for several compounds (e.g., estrone, androstenedione, testosterone; Figure 5).…”

“…In our experimental set-up, water was drawn from Kāne'ohe Bay, O'ahu and heated to 2.7° -3.2°C above ambient temperature in tanks at the Hawaiʻi Institute of Marine Biology [for details, see (11)]. Color scores, which are a proxy for algal abundance and coral health [i.e., a low score indicates bleaching (12)] were recorded for the ambient and stress treated nubbins ( Figure 1B).…”

“…Many advances have been made in identifying individual gene and metabolite markers of coral thermal stress (5), but little has been done to link these two omics data sources. This is explained by the complexity of holobiont metabolomic interactions, combined with the massive number of dark genes and dark metabolites in corals for which currently no function, and therefore no causal relationship exists (11). Approaches such as MAGI, which link metabolites and gene expression data to known biological pathways provides a foundation for studying non-model systems (10).…”

Applying model approaches in non-model systems: A review and case study on coral cell culture

“… 130 – 132 , and references therein] and toxicity [e.g. 133 – 135 ], a concrete list of coral “health” indicators has yet to be established [ 68 , 136 , 137 ]. Several main indicators of coral performance that are commonly applied at the colony or fragment level include: polyp activity [i.e.…”

Intrapopulation adaptive variance supports selective breeding in a reef-building coral

“…There was also a link between two loci strongly predictive of adult phenotype and amino acid modifications and metabolism, primarily via Betaine Glycine. Betaine Glycine is extremely common across the domains of life, abundant in corals 52,53 , and found in Montipora capitata Kāneʻohe Bay 52,54 . Betaine Glycine is an amino-acid osmolyte that has welldocumented protective effects on plants during abiotic stress and BG metabolism and biosynthesis pathways are found in corals 55 and commonly targeted in transgenic crop research 56 .…”