Diversity of Bile Salts in Fish and Amphibians: Evolution of a Complex Biochemical Pathway

Abstract

Bile salts are the major end-metabolites of cholesterol and are also important in lipid and protein digestion, as well as shaping of the gut microflora. Previous studies had demonstrated variation of bile salt structures across vertebrate species. We greatly extend prior surveys of bile salt variation in fish and amphibians, particularly in analysis of the biliary bile salts of Agnatha and Chondrichthyes. While there is significant structural variation of bile salts across all fish orders, bile salt profiles are generally stable within orders of fish and do not correlate with differences in diet. This large data set allowed us to infer evolutionary changes in the bile salt synthetic pathway. The hypothesized ancestral bile salt synthetic pathway, likely exemplified in extant hagfish, is simpler and much shorter than the pathway of most teleost fish and terrestrial vertebrates. Thus, the bile salt synthetic pathway has become longer and more complex throughout vertebrate evolution. Analysis of the evolution of bile salt synthetic pathways provides a rich model system for the molecular evolution of a complex biochemical pathway in vertebrates.

Intestinal synthesis and secretion of bile salts as an adaptation to developmental biliary atresia in the sea lamprey

“…Larval and adult lamprey are known to produce bile alcohol sulfates (26,28,43). Sulfation renders bile alcohols soluble, and enables their secretion.…”

The Gallbladder ofUranoscopus ScaberL. (Teleost Perciform Fish) is Lined by Specialized Cholecystocytes

“…The fatty acid levels in the blood are relatively low while the diet is lipid-rich (Plisetskaya, 1980), and, probably as in other Perciforms, the main bile components are phospholipids, cholic, and chenodeoxycholic acids along with 5b-bile alcohols (Moschetta et al, 2005;Hagey et al, 2010). Cholesterol nuclei could develop more easily from bile and cholecystocyte transport, because phospholipids appear generally absent in the bile of bony fish and most birds, while in mammals, the phospholipid to bile ratio varies widely among species.…”

The Essential Function of Genes for a Hydratase and an Aldehyde Dehydrogenase for Growth of Pseudomonas sp. Strain Chol1 with the Steroid Compound Cholate Indicates an Aldolytic Reaction Step for Deacetylation of the Side Chain

“…strain Chol1 as a model organism. Bile salts are surface-active steroid compounds that are produced and released by vertebrates to aid the digestion of lipophilic nutrients (18)(19)(20); in addition, bile salts can also act as pheromones in some aquatic vertebrates (21,22). The characterization of two transposon mutants of strain Chol1, which are unable to grow with cholate, showed that the degradation of the C 5 acyl side chain of cholate proceeds via the stepwise removal of an acetyl and a propionyl residue.…”