Characterizing the metabolic actions of natural stresses in the California red abalone, Haliotis rufescens using 1H NMR metabolomics

Abstract

Withering syndrome in California red abalone (Haliotis rufescens) is caused by the Rickettsiales-like prokaryote (WS-RLP) Candidatus Xenohaliotis californiensis. WS-RLP infection is not sufficient to cause withering syndrome, and for reasons not yet well understood additional stressors such as elevated water temperature appear to influence disease development. Using nuclear magnetic resonance (NMR) based metabolomics, we have investigated the influence of food availability, temperature, and bacterial infection, both individually and in combination, on the metabolic status of the red abalone. Food limitation caused dramatic reductions in all observed classes of foot muscle metabolites, while at the same time metabolite levels within the digestive gland were preserved or increased. We also found that food limitation in combination with elevated temperature led to greater metabolic perturbations in both tissue types than those observed under food limitation alone. WS-RLP infection and food-limitation resulted in many of the same metabolic changes within the tissues studied, although the effects of infection were less severe. We observed increased levels of homarine in the digestive gland of both food-limited and WS-RLP-infected animals, yet only observed increased homarine levels in the foot muscle of infected abalone. These results further support the recently established glucose-to-homarine ratio in foot muscle as a potential marker for differentiating WS-RLP-infected animals from those of both healthy and food limited abalone. Furthermore, we found that the NMR metabolic data correlates well with histological measurements supporting the use of the metabolomics approach for characterizing both normal and pathological events in marine species, particularly during periods of environmentally relevant stress.

Metabolomics: Methodologies and applications in the environmental sciences

“…A particular ratio of two metabolites (glucose and homarine) in foot muscle could serve as potential markers for differentiating the disease status of RLP infected animals. 12) Furthermore, the histological measurements also support the NMR metabolomics data in this study.…”

“…The metabolic studies highlight the characteristics of liver tumors in flatfish (dab, Limanda limanda) 1) and withering syndrome in red abalone (Haliotis rufescens) 10,12) versus corresponding healthy animals (Fig. 3).…”

“…Metabolomics can also help to determine the environmental factors leading to diseases such as withering syndrome in California red abalone, 12) since alone, Rickettsiales-like prokaryote (RLP) infection is not sufficient to cause withering syndrome. Other environmental stressors such as increased water temperature, acting in combination with RLP infection, have been shown to influence disease status.…”

“…8) Environmental scientists have also successfully applied metabolomics to examine toxic impacts or environmental stress on animals, [9][10][11] and to further develop biomarkers to diagnose diseases in wild animals. 1,12) It also demonstrates its importance in conjunction with other applications, like proteomics 1) and systems biology. 13) "Omics" can provide answers to questions surrounding biological effects that are caused by exposure to environmental stressors.…”

Ecological metabolomics: overview of current developments and future challenges

“…Recently, Larrainzar et al (2009), studying N 2 -fixation under drought conditions, observed a decrease in amino acids and sugar concentration and in the N 2 -fixation activity in roots of Medicago trunculata. Prior to this, Rosenblum et al (2005) used a 1 H NMR partial ecometabolic analysis to study the polar metabolites in red abalone, Haliotis rufenses, during infection by the rickettsia Candidants xenohaliotis californiensis under different levels of food sources. They concluded that food levels and other abiotic factors such as water temperature are responsible for disease development.…”