UC Davis

ABSTRACTThe Exxon Valdez oil spill occurred March 24, 1989, when herring were preparing to spawn in Prince William Sound. The herring population experienced an unanticipated, abrupt decline three years later, due–in part–to a mortality from infectious and parasitic diseases. Linking the oil spill to subsequent population collapse remains controversial. A major insight from years of studying the spill is that embryonic herring are profoundly sensitive to crude oil; exposure to vanishingly low levels of oil over a brief time early in a herring’s life-cycle can have long-lasting health effects, and oil exposure can disturb immune function. Could crude oil exposure during early life have compromised their immune system development, thereby increasing the risk of major disease outbreak in later life? To address this question, over the past few years we have sought to simulate the events surrounding the 1993 herring collapse using 1) experimental exposures to environmentally relevant levels of Alaska north slope crude oil, 2) fish from the Prince William Sound population and others, and 3) exposing fish in the laboratory to the same pathogens that caused the disease outbreak. To facilitate our investigation into the molecular effects of oil exposure on a non-traditional model organism, we sequenced and annotated a reference transcriptome for the Pacific herring, and conducted extensive research into a cost-effective, high-throughput RNA-sequencing library construction method for our samples. To that end we compared the effectiveness of two methods for generating sequencing libraries for gene expression analysis: 3'-end sequencing and whole transcript sequencing. We found similar levels of precision and power for detecting differentially expressed genes with both methods, but whole transcript sequencing performed better in non-traditional model species. Next, embryonic herring sourced from Prince William Sound, AK were exposed to a range of crude oil and transcriptomically interrogated across a detailed time-course, paying particular attention to heart and immune system development. We found that crude oil exposure disrupted cardiogenesis and caused heart defects in the developing fish, as well as modulated the immune system, causing dysregulation of gene expression. Finally, three geographically distinct populations of embryonic herring were exposed to low levels of oil, left to recover and grow-up in clean seawater, then exposed to pathogens. We found that an overall response to crude oil exposure in Pacific herring was determined by geography and not population history, with geographical distance playing a large role in molecular and phenotypic response to oil exposure. In conclusion, the Exxon Valdez oil spill may have contributed to the subsequent collapse of the herring population in Prince William Sound through compromising heart development and function in early development, causing long-lasting health effects. The research here shows that oil exposure to even low levels of crude oil can disrupt heart and potentially immune system development in embryonic herring, causing dysregulation in key genes involved in cardiogenesis, with the added insight that geographical distance plays a large role in the response to oil exposure.