Metabolomics Reveals Cryptic Interactive Effects of Species Interactions and Environmental Stress on Nitrogen and Sulfur Metabolism in Seagrass

Abstract

Eutrophication of estuaries and coastal seas is accelerating, increasing light stress on subtidal marine plants and changing their interactions with other species. To date, we have limited understanding of how such variations in environmental and biological stress modify the impact of interactions among foundational species and eventually affect ecosystem health. Here, we used metabolomics to assess the impact of light reductions on interactions between the seagrass Zostera marina, an important habitat-forming marine plant, and the abundant and commercially important blue mussel Mytilus edulis. Plant performance varied with light availability but was unaffected by the presence of mussels. Metabolomic analysis, on the other hand, revealed an interaction between light availability and presence of M. edulis on seagrass metabolism. Under high light, mussels stimulated seagrass nitrogen and energy metabolism. Conversely, in low light mussels impeded nitrogen and energy metabolism, and enhanced responses against sulfide toxicity, causing inhibited oxidative energy metabolism and tissue degradation. Metabolomic analysis thereby revealed cryptic changes to seagrass condition that could not be detected by traditional approaches. Our findings suggest that coastal eutrophication and associated reductions in light may shift seagrass-bivalve interactions from mutualistic to antagonistic, which is important for conservation management of seagrass meadows.

Additive response to multiple environmental stressors in the seagrass Zostera marina L.

“…The close agreement between the amount of available C and that incorporated into growth suggests that assimilation of was the major process by which was removed since the C contained in synthesized amino acids and proteins were included in our estimate of C allocated to growth. Our findings are supported by data from Castorani et al () and Hasler‐Sheetal et al () who found that eelgrass exposed to high light and high availability of (excreted from mussels) had sufficient energy to accumulate amino acids and grow well for about 4 weeks although the C‐reserves became depleted by the end.…”

“…High mobilization of C reserves combined with high acquisition of C resulted in the highest quantity of available C among all 2‐factor treatments. The amount of C allocated to growth constituted however less than 50% of the available C. We know of no studies that have evaluated the processes underlying the combined response to elevated heat and N, but we suggest that the remaining 50% of the available C was allocated to protection and repair processes in an attempt to alleviate the negative effects of HT (e.g., Bergmann et al ; Winters et al ; Gu et al ) while at the same time a significant amount of energy and C must have been used for assimilation of since these plants received the same N content as in those from the HN treatment (Marschner ; Villazán et al ; Hasler‐Sheetal et al ). The respiration rate in plants from the HT + HN treatment was similar to that in the control so any additional energetic expenditure related to these processes must either have taken place earlier in the experiment, or plants may alternatively have undergone structural alterations that could serve to reduce respiratory losses at the plant level.…”

“…Metabolomic studies on Z. marina support these findings: the quantities of sucrose, fructose, and most amino acids declined in plants exposed to shade for ca. 4 weeks, suggesting that insufficient energy was available for the synthesis of amino acids and proteins (Castorani et al ; Hasler‐Sheetal et al ). The total content of N in plants from our LL treatment remained largely the same over the course of the experiment and was nearly 100% higher than in the controls (Fig.…”

Metabolomics Reveals Cu(OH)2 Nanopesticide-Activated Anti-oxidative Pathways and Decreased Beneficial Antioxidants in Spinach Leaves

“…Na, Mg, P, K, Ca, Zn, Mn, Fe, Al, Cu, Mo, and Ag were analyzed using inductively coupled plasma mass spectrometry (ICP-MS 7900, Agilent). The standard solution was diluted from an ICP-MS environmental calibration standard (Agilent), which contains 1000 mg/L each of Fe, K, Ca, Na, Mg, and 10 mg/L each of Ag, Al, As, Ba, Be, Cd, Co, Cr, Cu, Mn, Mo, Ni, Pb, Sb, Se, Tl, V, Zn, Th, and U in 10% HNO 3 .…”

“…Some metabolites that play protective roles in abiotic or biotic stress responses were found more abundant in lettuce leaves exposed to Cu(OH) 2 nanopesticide. More recently, using gas chromatography− qualitative time-of-flight mass spectrometry (GC−qTOF-MS)-based metabolomics, Hasler-Sheetal et al 3 revealed cryptic metabolic changes of seagrass (Zostera marina) and bivalve interactions under reduced-light conditions, which could not be detected by traditional approaches. Thus, metabolomics can provide a more-sensitive and mechanistic understanding of biological response to a particular stressor.…”