Graduate Thesis Or Dissertation

 

The Ecophysiology of Thiamine Deficiency Complex : Evaluating Sources of Thiaminase in Great Lakes Food Webs Public Deposited

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  • Thiamine (vitamin B₁) is required by all living organisms for carbohydrate metabolism and synthesis of amino acids. Thiamine deficiency is responsible for several related classes of early life stage mortality disorders in salmonines, including Thiamine Deficiency Complex (TDC) in the Laurentian Great Lakes, Cayuga Syndrome in the Finger Lakes, and the M74 in the Baltic Sea. TDC is caused not by lack of sufficient intake of thiamine but rather by a diet rich in prey that contain thiaminase, a thiamine-degrading enzyme. TDC caused by ingestion of thiaminase-containing prey occurs in these wild fish populations and has also been observed in mink, foxes, seals, alligators, chickens, and ruminants. TDC is one of several impediments to rehabilitation of Lake Trout (Salvelinus namaycush), the native apex predator in the Great Lakes. The proximate cause of TDC is known to be the ingestion of prey fish containing high levels of thiaminase, specifically Alewife (Alosa pseudoharengus) and Rainbow Smelt (Osmerus mordax); however, the ultimate source of thiaminase in thiaminase-containing fishes remains unknown. Evaluating potential sources of thiaminase in fishes is essential for understanding thiaminase trophodynamics and developing management strategies for mitigating TDC and facilitating rehabilitation of Lake Trout populations. Thiaminase in prey fishes is hypothesized to originate from two possible sources: either thiaminase-containing fishes acquire thiaminase from their diet (dietary acquisition hypothesis) or thiaminase-containing fishes make the thiaminase enzyme themselves (de novo synthesis hypothesis); these two hypotheses are not mutually exclusive. Chapter 1 describes the causes of TDC and why characterization of the sources of thiaminase in aquatic food webs is necessary. The three primary data chapters presented herein describe whole food web investigations that seek to determine the source of thiaminase in Great Lakes fishes. In Chapter 2, zooplankton were evaluated as a potential source of dietarily acquired thiaminase activity by comparing the thiaminase activity in bulk zooplankton to the zooplankton community composition. Three types of multivariate analysis revealed one candidate source of thiaminase activity, Ploesoma, an omnivorous loricate rotifer. Despite the apparent correlation between Ploesoma biomass and thiaminase activity in bulk zooplankton, Ploesoma spp. constituted sufficiently low biomass that its thiaminase activity would have to be extraordinarily high (i.e., at unprecedented levels) to constitute the major source of thiaminase in Great Lakes food webs. Furthermore, Ploesoma was never observed in the diet of thiaminase-containing fish. Therefore Ploesoma is an unlikely source of thiaminase. No other component of the zooplankton community was consistently related to thiaminase activity. In Chapter 3, the thiaminase activity in fishes was assessed in relation to species, season, depth, and location of capture, and the dietary acquisition hypothesis was assessed directly using stomach content and fatty acid signature analysis. Thiaminase activity was higher in spring than in summer and fall. Round Goby (Neogobius melanostomus) thiaminase activity was higher than previously reported, and Slimy Sculpin (Cottus cognatus) thiaminase activity was highly variable, sometimes exceeding that of Rainbow Smelt. The dietary acquisition hypothesis was evaluated by comparing the thiaminase activity in fish viscera to both the diets and fatty acid signatures of fishes. No compelling evidence that thiaminase activity of fish viscera was consistently the result of consumption of any specific prey taxa was found using three types of multivariate analyses. Indicator Species Analysis suggested Bythotrephes as a potential candidate source of thiaminase, but Bythotrephes was not consumed by some fishes with high thiaminase activity. If the source of thiaminase activity is dietary, the source may be Bythotrephes for some fishes, but those that did not consume Bythotrephes would need to obtain thiaminase from a different source. Fatty acid analysis suggested a moderate tendency for higher thiaminase activity in pelagically-feeding rather than benthically-feeding fishes, but several pelagically feeding fishes contained undetectable thiaminase activity and some benthically feeding fishes contained thiaminase activity comparable to or greater than pelagically feeding fishes. Together, this evidence indicated that no specific prey item was consistently related to thiaminase activity. In Chapter 4, the de novo hypothesis was assessed directly using two approaches. The first approach compared the biochemical characteristics of thiaminases in Alewife, Carp (Cyprinus carpio), quagga mussels (Dreissena rostriformis bugensis), and a bacterium (Paenibacillus thiaminolyticus) that has been isolated from the intestines of Alewife and is known to produce thiaminase. Thiaminases in these four organisms vary in their mass, migration characteristics, tolerance to denaturation, and isoelectric points, suggesting that the source of thiaminase differs in these four taxa. The second approach identified candidate thiaminase genes in fishes using existing information from small peptide fragments from two fish thiaminases from partially purified from Carp and Red Cornetfish (Fistularia petimba). Candidate genes in Carp, Zebrafish (Danio rerio), and Alewife that were homologous to the known peptide fragments were identified, synthesized, and overexpressed. The Zebrafish candidate gene produced an active thiaminase enzyme. This finding confirms de novo synthesis and represents the first report of a thiaminase-encoding protein in any multicellular organism. The candidate gene identified for Alewife is predicted to produce a protein product with biochemical properties that match those determined empirically. The dietary acquisition hypothesis was not well-supported, and findings from Chapters 2 and 3 did not converge as would be expected if the source of thiaminase was dietarily acquired. The potential for de novo synthesis by fishes was confirmed experimentally, which represents the first report of a gene for a thiaminase enzyme from a multicellular animal. Future research should focus on confirming that de novo production accounts for the thiaminase activity in fishes and understanding the physiological factors that lead to increased thiaminase production. This work is relevant to fishery managers in affected ecosystems (Great Lake, Baltic Sea, Finger Lakes, NY) and to biochemists and nutritionist interested in thiamine metabolism.
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  • 2017-08-04 to 2018-09-21

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