Animal degradation of microbial storage polyhydroxyalkanoates.

Abstract

A wide range of microorganisms produce storage biopolymer polyhydroxyalkanoates (sPHAs) as carbon and energy reserves. However, only bacteria and fungi are known to degrade microbial sPHAs, using enzymes called polyhydroxyalkanoate depolymerases (PHADs). Here we show that some animals also have PHADs that can degrade sPHAs. We discovered a PHAD in the gutless oligochaete Olavius algarvensis, a marine worm that gains nutrition by digesting bacterial symbionts, including a dominant symbiont in which sPHAs account for up to 42% of cellular carbon stores. Enzyme assays, combined with mass spectrometry, confirmed that heterologously expressed O. algarvensis PHAD degraded sPHAs into hydroxyalkanoate monomers that can enter conserved metabolic pathways. Imaging of mRNA showed that PHAD was expressed in the oligochaete epidermis, the site of symbiont digestion. We further identified PHADs in more than 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 PHADs. Functional assays confirmed that PHADs from phylogenetically distant animal lineages spanning aquatic and terrestrial environments degrade sPHAs. These findings reveal a previously unrecognized pathway by which protists and animals can access microbial carbon reserves, with broad relevance given the widespread occurrence of sPHAs across ecosystems.