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Ecotoxico-lipidomics: An emerging concept to understand chemical-metabolic relationships in comparative fish models.

ABSTRACT: Lipids play an essential role in development, homeostatic functions, immune signaling, reproduction, and growth. Although it is evident that changes in lipid biosynthesis and metabolism can affect organismal physiology, few studies have determined how environmental stressors affect lipid pathways, let alone alter global lipid profiles in fish. This is a significant research gap, as a number of environmental contaminants interact with lipid signaling and metabolic pathways. In this review, we highlight the utility of lipidomics as a tool in environmental toxicology, discussing the current state of knowledge regarding chemical-lipidomic perturbations. As with most oviparous animals, the processing and storage of lipids during oocyte development is also particularly important for embryogenesis in fish. Using largemouth bass (Micropterus salmoides) as an example, transcriptomics data suggest that various chemicals alter lipid metabolism and regulation, highlighting the need for more sophisticated investigations into how toxicants impact lipid responses. We also point out the challenges ahead; these include a lack of understanding about lipid processing and signaling in fish, tissue and species-specific lipid composition, and extraneous factors (e.g., nutrition, temperature) that confound interpretation. For example, toxicant exposure can lead to oxidative stress and lipid peroxidation, resulting in complex lipid byproducts that are challenging to measure. With the emergence of lipidomics in systems toxicology, multi-omics approaches are expected to more clearly define effects on physiology, creating stronger linkages between multiple molecular entities (gene-protein-lipid/metabolite). The development and implementation of novel technologies such as ion mobility-mass spectrometry and ozone-induced dissociation support the complete structural elucidation of lipid molecules. This has implications in the adverse outcome pathway framework, which will enhance the application of lipidomics in toxicology by linking these molecular changes to effects at higher levels of biological organization.

SUBMITTER: Dreier DA

PROVIDER: S-EPMC7669741 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Flavobacterium spartansii strain T16T was isolated from a disease outbreak in hatchery-reared Chinook salmon (Oncorhynchus tshawytscha) fingerlings. To gain insight into its genomic content, structure and virulence pathogenesis factors, comparative genome analyses were performed using genomes from environmental and virulent Flavobacterium strains. F. spartansii shared low average nucleotide identity (ANI) to well-known fish-pathogenic flavobacteria (e.g., F. columnare, F. psychrophilum, and F. branchiophilum), indicating that it is a new and emerging fish pathogen. The genome in T16T had a length of 5,359,952 bp, a GC-content 35.7%, and 4,422 predicted protein-coding sequences. Flavobacterium core genome analysis showed that the number of shared genes decreased with the addition of input genomes and converged at 1182 genes. At least 8 genomic islands and 5 prophages were predicted in T16T. At least 133 virulence factors associated with virulence in pathogenic bacteria were highly conserved in F. spartansii T16T. Furthermore, genes linked to virulence in other bacterial species (e.g., those encoding for a type IX secretion system, collagenase and hemolysin) were found in the genome of F. spartansii T16T and were conserved in most of the analyzed pathogenic Flavobacterium. F. spartansii was resistant to ampicillin and penicillin, consistent with the presence of multiple genes encoding diverse lactamases and the penicillin-binding protein in the genome. To allow for future investigations into F. spartansii virulence in vivo, a transposon-based random mutagenesis strategy was attempted in F. spartansii T16T using pHimarEm1. Four putative gliding motility deficient mutants were obtained and the insertion sites of pHimarEm1 in the genome of these mutants were characterized. In total, study results clarify some of the mechanisms by which emerging flavobacterial fish pathogens may cause disease and also provide direly needed tools to investigate their pathogenesis.

Project description:BACKGROUND:Glucose plays a key role as an energy source in most mammals, but its importance in fish appears to be limited that so far seemed to belong to diabetic humans only. Several laboratories worldwide have made important efforts in order to better understand this strange phenotype observed in fish. However, the mechanism of carbohydrate/glucose metabolism is astonishingly complex. Why basal glycaemia is different between fish and mammals and how carbohydrate metabolism is different amongst organisms is largely uncharted territory. The utilization of comparative systems biology with model vertebrates to explore fish metabolism has become an essential approach to unravelling hidden in vivo mechanisms. RESULTS:In this study, we first built a database containing 791, 593, 523, 666 and 698 carbohydrate/glucose metabolic genes from the genomes of Danio rerio, Xenopus tropicalis, Gallus gallus, Mus musculus and Homo sapiens, respectively, and most of these genes in our database are predicted to encode specific enzymes that play roles in defined reactions; over 57% of these genes are related to human type 2 diabetes. Then, we systematically compared these genes and found that more than 70% of the carbohydrate/glucose metabolic genes are conserved in the five species. Interestingly, there are 4 zebrafish-specific genes (si:ch211-167b20.8, CABZ01043017.1, socs9 and eif4e1c) and 1 human-specific gene (CALML6) that may alter glucose utilization in their corresponding species. Interestingly, these 5 genes are all carbohydrate regulation factors, but the enzymes themselves are involved in insulin regulation pathways. Lastly, in order to facilitate the use of our data sets, we constructed a glucose metabolism database platform ( http://101.200.43.1:10000/ ). CONCLUSIONS:This study provides the first systematic genomic insights into carbohydrate/glucose metabolism. After exhaustive analysis, we found that most metabolic genes are conserved in vertebrates. This work may resolve some of the complexities of carbohydrate/glucose metabolic heterogeneity amongst different vertebrates and may provide a reference for the treatment of diabetes and for applications in the aquaculture industry.

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Ecotoxico-lipidomics: An emerging concept to understand chemical-metabolic relationships in comparative fish models.

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