Evolutionary and ecological correlates of thiaminase in fishes
Abstract Thiamine (vitamin B1) is required by all living organisms in multiple metabolic pathways. It is scarce in natural systems, and deficiency can lead to reproductive failure, neurological issues, and death. One major cause of thiamine deficiency is an overreliance on diet items containing the...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-10-01
|
| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-023-44654-x |
| _version_ | 1797452753951260672 |
|---|---|
| author | Freya E. Rowland Catherine A. Richter Donald E. Tillitt David M. Walters |
| author_facet | Freya E. Rowland Catherine A. Richter Donald E. Tillitt David M. Walters |
| author_sort | Freya E. Rowland |
| collection | DOAJ |
| description | Abstract Thiamine (vitamin B1) is required by all living organisms in multiple metabolic pathways. It is scarce in natural systems, and deficiency can lead to reproductive failure, neurological issues, and death. One major cause of thiamine deficiency is an overreliance on diet items containing the enzyme thiaminase. Thiaminase activity has been noted in many prey fishes and linked to cohort failure in salmonid predators that eat prey fish with thiaminase activity, yet it is generally unknown whether evolutionary history, fish traits, and/or environmental conditions lead to production of thiaminase. We conducted literature and GenBank BLAST sequence searches to collect thiaminase activity data and sequence homology data in expressed protein sequences for 300 freshwater and marine fishes. We then tested whether presence or absence of thiaminase could be predicted by evolutionary relationships, trophic level, omega-3 fatty acid concentrations, habitat, climate, invasive potential, and body size. There was no evolutionary relationship with thiaminase activity. It first appears in Class Actinoptergyii (bony ray-finned fishes) and is present across the entire Actinoptergyii phylogeny in both primitive and derived fish orders. Instead, ecological factors explained the most variation in thiaminase: fishes were more likely to express thiaminase if they fed closer to the base of the food web, were high in polyunsaturated fatty acids, lived in freshwater, and were from tropical climates. These data provide a foundation for understanding sources of thiaminase leading to thiamine deficiency in fisheries and other organisms, including humans that eat uncooked fish. |
| first_indexed | 2024-03-09T15:13:14Z |
| format | Article |
| id | doaj.art-f0155c5e14bd407fadd172ac21eb090b |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-03-09T15:13:14Z |
| publishDate | 2023-10-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-f0155c5e14bd407fadd172ac21eb090b2023-11-26T13:15:44ZengNature PortfolioScientific Reports2045-23222023-10-011311910.1038/s41598-023-44654-xEvolutionary and ecological correlates of thiaminase in fishesFreya E. Rowland0Catherine A. Richter1Donald E. Tillitt2David M. Walters3U.S. Geological Survey, Columbia Environmental Research CenterU.S. Geological Survey, Columbia Environmental Research CenterU.S. Geological Survey, Columbia Environmental Research CenterU.S. Geological Survey, Columbia Environmental Research CenterAbstract Thiamine (vitamin B1) is required by all living organisms in multiple metabolic pathways. It is scarce in natural systems, and deficiency can lead to reproductive failure, neurological issues, and death. One major cause of thiamine deficiency is an overreliance on diet items containing the enzyme thiaminase. Thiaminase activity has been noted in many prey fishes and linked to cohort failure in salmonid predators that eat prey fish with thiaminase activity, yet it is generally unknown whether evolutionary history, fish traits, and/or environmental conditions lead to production of thiaminase. We conducted literature and GenBank BLAST sequence searches to collect thiaminase activity data and sequence homology data in expressed protein sequences for 300 freshwater and marine fishes. We then tested whether presence or absence of thiaminase could be predicted by evolutionary relationships, trophic level, omega-3 fatty acid concentrations, habitat, climate, invasive potential, and body size. There was no evolutionary relationship with thiaminase activity. It first appears in Class Actinoptergyii (bony ray-finned fishes) and is present across the entire Actinoptergyii phylogeny in both primitive and derived fish orders. Instead, ecological factors explained the most variation in thiaminase: fishes were more likely to express thiaminase if they fed closer to the base of the food web, were high in polyunsaturated fatty acids, lived in freshwater, and were from tropical climates. These data provide a foundation for understanding sources of thiaminase leading to thiamine deficiency in fisheries and other organisms, including humans that eat uncooked fish.https://doi.org/10.1038/s41598-023-44654-x |
| spellingShingle | Freya E. Rowland Catherine A. Richter Donald E. Tillitt David M. Walters Evolutionary and ecological correlates of thiaminase in fishes Scientific Reports |
| title | Evolutionary and ecological correlates of thiaminase in fishes |
| title_full | Evolutionary and ecological correlates of thiaminase in fishes |
| title_fullStr | Evolutionary and ecological correlates of thiaminase in fishes |
| title_full_unstemmed | Evolutionary and ecological correlates of thiaminase in fishes |
| title_short | Evolutionary and ecological correlates of thiaminase in fishes |
| title_sort | evolutionary and ecological correlates of thiaminase in fishes |
| url | https://doi.org/10.1038/s41598-023-44654-x |
| work_keys_str_mv | AT freyaerowland evolutionaryandecologicalcorrelatesofthiaminaseinfishes AT catherinearichter evolutionaryandecologicalcorrelatesofthiaminaseinfishes AT donaldetillitt evolutionaryandecologicalcorrelatesofthiaminaseinfishes AT davidmwalters evolutionaryandecologicalcorrelatesofthiaminaseinfishes |