Similar Enzymatic Functions in Distinct Bioluminescence Systems: Evolutionary Recruitment of Sulfotransferases in Ostracod Light Organs

Genes from ancient families are sometimes involved in the convergent
evolutionary origins of similar traits, even across vast phylogenetic
distances. Sulfotransferases are an ancient family of enzymes that
transfer sulfate from a donor to a wide variety of substrates, including
probable roles in some bioluminescence systems. Here we demonstrate
multiple sulfotransferases, highly expressed in light organs of the
bioluminescent ostracod Vargula tsujii, transfer sulfate in vitro to the
luciferin substrate, vargulin. We find luciferin sulfotransferases of
ostracods are not orthologous to known luciferin sulfotransferases of
fireflies or sea pansies; animals with distinct and convergently evolved
bioluminescence systems compared to ostracods. Therefore, distantly
related sulfotransferases were independently recruited at least three
times, leading to parallel evolution of luciferin metabolism in three
highly diverged organisms. Re-use of homologous genes is surprising in
these bioluminescence systems because the other components, including
luciferins and luciferases, are completely distinct. Whether convergently
evolved traits incorporate ancient genes with similar functions or instead
use distinct, often newer, genes may be constrained by how many genetic
solutions exist for a particular function. When fewer solutions exist, as
in genetic sulfation of small molecules, evolution may be more constrained
to use the same genes time and again.