Metabolomic Profiles of the Creeping Wood Sorrel Oxalis corniculata in Radioactively Contaminated Fields in Fukushima: Dose-Dependent Changes in Key Metabolites

Abstract

The biological impacts of the Fukushima nuclear accident, in 2011, on wildlife have been studied in many organisms, including the pale grass blue butterfly and its host plant, the creeping wood sorrel Oxalis corniculata. Here, we performed an LC–MS-based metabolomic analysis on leaves of this plant collected in 2018 from radioactively contaminated and control localities in Fukushima, Miyagi, and Niigata prefectures, Japan. Using 7967 peaks detected by LC–MS analysis, clustering analyses showed that nine Fukushima samples and one Miyagi sample were clustered together, irrespective of radiation dose, while two Fukushima (Iitate) and two Niigata samples were not in this cluster. However, 93 peaks were significantly different (FDR < 0.05) among the three dose-dependent groups based on background, low, and high radiation dose rates. Among them, seven upregulated and 15 downregulated peaks had single annotations, and their peak intensity values were positively and negatively correlated with ground radiation dose rates, respectively. Upregulated peaks were annotated as kudinoside D (saponin), andrachcinidine (alkaloid), pyridoxal phosphate (stress-related activated vitamin B6), and four microbe-related bioactive compounds, including antibiotics. Additionally, two peaks were singularly annotated and significantly upregulated (K1R1H1; peptide) or downregulated (DHAP(10:0); decanoyl dihydroxyacetone phosphate) most at the low dose rates. Therefore, this plant likely responded to radioactive pollution in Fukushima by upregulating and downregulating key metabolites. Furthermore, plant-associated endophytic microbes may also have responded to pollution, suggesting their contributions to the stress response of the plant.

Ingestional Toxicity of Radiation-Dependent Metabolites of the Host Plant for the Pale Grass Blue Butterfly: A Mechanism of Field Effects of Radioactive Pollution in Fukushima

“…This field-laboratory paradox was explained by the field effect hypothesis: the host plant in the field responded to low-level radiation stress by upregulating metabolites that were toxic to larvae as a part of plant defense mechanisms [ 59 , 67 ]. Subsequent studies have reported upregulated and downregulated metabolites and nutrients in plant leaves [ 48 , 49 , 50 ], supporting this field effect hypothesis.…”

“…The Fukushima nuclear accident was reported to have caused various biological and ecological effects on animals, such as birds [ 31 , 32 , 33 ], insects [ 34 , 35 , 36 , 37 , 38 , 39 ], Japanese monkeys [ 40 , 41 , 42 ], and intertidal invertebrates [ 43 ], plants such as rice [ 44 , 45 ], fir trees [ 46 ], red pine trees [ 47 ], and the creeping wood sorrel Oxalis corniculata [ 48 , 49 , 50 ], and soil microbes [ 51 ]. A series of our studies [ 31 , 32 , 33 , 34 , 52 , 53 , 54 , 55 , 56 , 57 , 58 , 59 , 60 , 61 , 62 , 63 ] demonstrated that the pale grass blue butterfly has been severely affected by the Fukushima nuclear accident.…”

“…Accordingly, ikarugamycin detected from leaves of O. corniculata is likely from an endophytic Streptomyces sp. in leaves or roots, which responded to low-level radiation [ 49 , 50 ]. Ikarugamycin and its derivatives are antifungal [ 89 ] and antibacterial [ 89 , 90 ] agents and inhibit clathrin-mediated endocytosis in eukaryotic cell lines [ 91 ].…”

The Plastic Larval Body Color of the Pale Grass Blue Butterfly Zizeeria maha (Lepidoptera: Lycaenidae) in Response to the Host Plant Color: The Maternal Effect on Crypsis

“…Similar to other lycaenid butterflies, the pale grass blue butterfly sequesters flavonoids from the host plant leaves in the wing scales [ 78 , 79 ]. Creeping wood sorrel contains pigments (such as carotenoids and flavonoids) and other secondary metabolites [ 78 , 79 , 80 , 81 , 82 ]. There is a reasonable possibility that the maternal effects detected in the present study may be caused by the deposition of flavonoid precursors in eggs by mothers.…”

The second decade of the blue butterfly in Fukushima: Untangling the ecological field effects after the Fukushima nuclear accident

“…Secondary metabolites were further examined in the plant collected from contaminated fields in Fukushima (Sakauchi et al, 2022). Again, stress‐related metabolites were upregulated.…”