Animals degrade the biopolymer polyhydroxyalkanoate

Abstract

The biopolymer polyhydroxyalkanoate (PHA) is a valuable carbon and energy source. However, only bacteria and fungi are currently known to degrade PHA, using an enzyme called PHA depolymerase (PHAD). Here, we showed that animals also have a PHAD that can degrade PHA. We discovered a PHAD in the gutless oligochaete, Olavius algarvensis. These marine worms gain their nutrition by digesting their bacterial symbionts, with PHA making up to 42% of the carbon in their dominant symbiont. Enzyme assays with a heterologously expressed O. algarvensis PHAD confirmed that it degraded PHA. Imaging of mRNA showed that PHAD was expressed in the oligochaete’s epidermis, the site of symbiont digestion. Comparative sequence analyses revealed that PHADs are present in all other 14 gutless oligochaetes species examined. Moreover, we also found PHADs in over 66 gut-bearing animal species from nine phyla and 19 protist species from three major supergroups, suggesting that the last common ancestor of metazoans possessed a PHAD. Given how widespread PHADs are in protists and animals, and the ubiquity of microbially produced PHA in terrestrial and aquatic environments, the ability of protists and animals to degrade PHA could play a previously unrecognized role in carbon cycling.