Evolutionary diversity of bile salts in reptiles and mammals, including analysis of ancient human and extinct giant ground sloth coprolites

Abstract

BackgroundBile salts are the major end-metabolites of cholesterol and are also important in lipid and protein digestion and in influencing the intestinal microflora. We greatly extend prior surveys of bile salt diversity in both reptiles and mammals, including analysis of 8,000 year old human coprolites and coprolites from the extinct Shasta ground sloth (Nothrotherium shastense).ResultsWhile there is significant variation of bile salts across species, bile salt profiles are generally stable within families and often within orders of reptiles and mammals, and do not directly correlate with differences in diet. The variation of bile salts generally accords with current molecular phylogenies of reptiles and mammals, including more recent groupings of squamate reptiles. For mammals, the most unusual finding was that the Paenungulates (elephants, manatees, and the rock hyrax) have a very different bile salt profile from the Rufous sengi and South American aardvark, two other mammals classified with Paenungulates in the cohort Afrotheria in molecular phylogenies. Analyses of the approximately 8,000 year old human coprolites yielded a bile salt profile very similar to that found in modern human feces. Analysis of the Shasta ground sloth coprolites (approximately 12,000 years old) showed the predominant presence of glycine-conjugated bile acids, similar to analyses of bile and feces of living sloths, in addition to a complex mixture of plant sterols and stanols expected from an herbivorous diet.ConclusionsThe bile salt synthetic pathway has become longer and more complex throughout vertebrate evolution, with some bile salt modifications only found within single groups such as marsupials. Analysis of the evolution of bile salt structures in different species provides a potentially rich model system for the evolution of a complex biochemical pathway in vertebrates. Our results also demonstrate the stability of bile salts in coprolites preserved in arid climates, suggesting that bile salt analysis may have utility in selected paleontological research.

3,4-Seco-12α-hydroxy-5β-cholan-3,4,24-trioic Acid, a Novel Secondary Bile Acid: Isolation from the Bile of the Common Ringtail Possum (Pseudocheirus peregrinus) and Chemical Synthesis

“…The 1α-hydroxy derivative (1α-OH-CDCA) of Chenodeoxycholic Acid (CDCA) was shown to be the major bile acid in the Australian opossum Trichosurus vulpecula (Lesson), and dubbed vulpecholic acid [26,27]. This bile acid was also identified in the biliary bile acids of the spotted cuscus (Phalanger maculatus), and 1β-hydroxy-CDCA was identified in the biliary bile acids of the feather-tailed glider (Acrobates pygmaeus) [6].…”

“…It is apparent that the switch from bile alcohols to bile acids, and the utilization of taurine for conjugation had already occurred in marsupials far earlier in time than the last common precursor of marsupials and eutherian mammals (estimated to be more than 100 million years ago). Currently, the marsupial lineage is an active site of bile acid evolution, with different species exhibiting new and structurally unique bile salts as noted above [1,2,5,6]. …”

“…In the Queensland kaola (Pascolarctos adjustus), the kowari (Dasyuroides byrnei) and the spotted-tailed quoll (Dasyrus maculatus), 7-oxo-lithocholic acid (3α-hydroxy-7-oxo-5β-cholan-24-oic acid) is a dominant biliary bile acid [6].…”

“…Haslewood proposed that bile acid structure provides additional phenotypic information for the establishment of phylogenetic relationships [4], and we have extended his pioneering work in a series of papers [5][6][7].…”

Use of Chromatography in Animal Ecology

“…Bile acids are produced by all vertebrates and show a great structural diversity among different species [9,10]. Indeed, no other class of small molecules shows such striking variety across vertebrates.…”