Branched-chain amino acid assimilation enables mixotrophy of ammonia-oxidizing archaeal sponge symbionts

Abstract

Marine sponges and ammonia-oxidizing archaea (AOA) represent one of the earliest animal-microbe symbioses. AOA are considered metabolically constrained chemolithoautotrophs that remove nitrogenous waste within the sponge holobiont. Here, we expand this view by demonstrating that symbiotic AOA assimilate branched-chain amino acids (BCAA) as additional carbon and nitrogen sources. By combining stable isotope probing with fluorescence and chemical imaging, we trace the assimilation of 13C- and 15N-labeled BCAA (leucine, isoleucine, and valine) in the sponge holobiont Ianthella basta at single-cell resolution. We show that the ability to take up, degrade, and biosynthesize BCAA is a common adaptation among symbiotic AOA lineages. This ability may enable symbiotic AOA to modulate BCAA concentrations in their auxotrophic sponge hosts. Modulation of BCAA availability by symbionts may regulate the leucine-sensitive mTOR (mechanistic target of rapamycin) signaling pathway in sponges.