Seasonal Variations and Interspecific Differences in Metabolomes of Freshwater Fish Tissues: Quantitative Metabolomic Profiles of Lenses and Gills

Abstract

This work represents the first comprehensive report on quantitative metabolomic composition of tissues of pike-perch (Sander lucioperca) and Siberian roach (Rutilus rutilus lacustris). The total of 68 most abundant metabolites are identified and quantified in the fish lenses and gills by the combination of LC-MS and NMR. It is shown that the concentrations of some compounds in the lens are much higher than that in the gills; that indicates the importance of these metabolites for the adaptation to the specific living conditions and maintaining the homeostasis of the fish lens. The lens metabolome undergoes significant seasonal changes due to the variations of dissolved oxygen level and fish feeding activity. The most season-affected metabolites are osmolytes and antioxidants, and the most affected metabolic pathway is the histidine pathway. In late autumn, the major lens osmolytes are N-acetyl-histidine and threonine phosphoethanolamine (Thr-PETA), while in winter the highest concentrations were observed for serine phosphoethanolamine (Ser-PETA) and myo-inositol. The presence of Thr-PETA and Ser-PETA in fish tissues and their role in cell osmotic protection are reported for the first time. The obtained concentrations can be used as baseline levels for studying the influence of environmental factors on fish health.

Most abundant metabolites in tissues of freshwater fish pike-perch (Sander lucioperca)

“…The major antioxidant of the fish lens is OSH 12 . It has been shown that the level of OSH in S. lucioperca lens vary from 3 µmol/g at autumn to 1.5 µmol/g at winter 15 , which is in a good agreement with our present data ( Table 1). The concentration of the second most abundant lens antioxidant, GSH, is 3-4 times lower than that of OSH.…”

“…We found in the fish tissues the following compounds with antioxidative properties: glutathione (GSH), ascorbate, OSH, and NADH. The detection of minor amounts of one more well-known thiol antioxidant, ergothioneine, in the gills of another freshwater fish, R. rutilus lacustris, has recently been reported 15 ; however, in the present work ergothioneine was not found neither by NMR nor by LC-MS in any of the studied tissues of S. lucioperca. NADH was found only in NMR spectra of liver, muscle, heart, and lens, and its concentration in these tissues does not exceed 15 nmol/g.…”

“…The lens osmolytes are myo-inositol, NAH, NAA, Thr-PETA, and Ser-PETA. We have previously shown 15 that the concentrations of osmolytes in the fish lens undergo significant seasonal variations. At the late winter time, when the fish was caught for this study, the most abundant lens osmolyte is myo-inositol.…”

Gametogenesis-Related Fluctuations in Ovothiol Levels in the Mantle of Mussels from Different Estuaries: Fighting Oxidative Stress for Spawning in Polluted Waters

“…Metabolite enrichment analysis and pathway analysis showed the pathways establishing main differences between analyzed "experimental" groups, these including all analyses involving ovaries from Arriluze the histidine metabolism and the glutathione metabolism pathways. In a recent work by Tsentalovich et al [33], the lens-and gill-specific metabolite profiles in two freshwater fish species highlighted the histidine and glutathione metabolism pathways among the most impacted ones when comparing two different sampling seasons. The only vertebrates to present the ovoA gene in their genomes are chondrichthyans [9,15], but it has been proven that OSH-A is accumulated in some fish cells and tissues, including oocytes in salmons [1], and very importantly, the lens in different species [33,34].…”

“…Probably, teleosts and other vertebrates accumulate OSH-A through the diet. Quantification of the levels of metabolites (combination of liquid chromatography -LC-, mass spectrometry -MS-, and nuclear magnetic resonance -NMR-) in freshwater fish lenses revealed that OSH-A it is the most important antioxidant present, and that when concentrations of OSH-A increase in autumn in comparison to winter, it occurs together with increased levels of GSH [33]. OSH-A is the result of the conjugation of cysteine and histidine, so that could be one of the drivers of the observed alterations in the histidine and cysteine metabolism pathways in mussel mantles.…”