Spatial lipidomics suggests fatty acid scavenging by an intranuclear parasite

Bacteria of the family Endozoicomonadaceae are widely associated with marine animals, yet their in situ metabolism remains mostly unknown. Genomic studies suggest that members of this family engage in extensive metabolic exchange with their hosts, ranging from nutrient provision in mutualistic sponge and coral symbioses to strong dependence on host metabolites like lipids in parasitic associations. Here, we study the lipid phenotype of the parasitic bacterium Candidatus Endonucleibacter childressi in its native tissue environment. The bacterium infects epithelial cells in the gill of the deep-sea mussel Gigantidas childressi and co-occurs with the mussel chemosynthetic symbionts providing a system to compare lipid profiles of symbiotic and parasitic gammaproteobacteria. We linked bacterial identity to metabolic phenotypes by combining mass spectrometry imaging with 16S rRNA fluorescence in situ hybridization. We identified phospholipids characteristic of regions infected with Ca. Endonucleibacter childressi. A subset of these lipids was also detected in symbiont-colonized regions, revealing a partial overlap in the phospholipid profiles of the two gammaproteobacteria. Fatty acids from PEs assigned to Ca. Endonucleibacter childressi contained polyunsaturated fatty acids such as FA 16:3, FA 18:3 or FA 18:4 which have not been reported from cultured close relatives. We hypothesize that the observed fatty acid profile may reflect adaptations to a host-associated lifestyle which involves the acquisition and remodeling of host-derived fatty acids. Our findings demonstrate the value of characterizing bacterial metabolic phenotypes directly in their native tissue environment and highlight the potential of spatial lipidomics to reveal metabolic dependencies in host-microbe associations.