Giant sulfur bacteria host intracellular endobionts

Abstract

Eukaryotic organelles, such as mitochondria and chloroplasts, are thought to be 12 derived from symbiotic bacteria that were hosted by a proto-eukaryotic microbe in the 13 deep evolutionary past. Despite their potential relevance to eukaryote evolution, 14 endosymbiotic relationships involving free-living, viable bacterial or archaeal host cells, 15 have not been previously established in the modern biosphere. Here we show that some 16 populations of the largest known bacteria, Candidatus Thiomargarita spp., host bacterial 17 populations within their cells, providing a singular example of a free-living marine 18 bacterium that hosts endobiont bacteria. Multiple lines of evidence show that the host and 19 endobiont cells are metabolically active. The phylogeny of these endobiont bacteria places 20 them within a clade that includes known animal endosymbionts – specifically 21 gammaproteobacteria that live within siboglinid tubeworms. Metagenomic results indicate 22 that the metabolism of the endobionts is remarkably similar to that of the host Ca. 23 Thiomargarita cells, which are known for their remarkable ability to store metabolites 24 such as nitrate, suggesting a potentially parasitic, rather than mutualistic, relationship. In 25 addition to establishing the viability of a host bacterium with endobiont bacteria, these 26 findings extend the range of hosts for sulfide-oxidizing endosymbionts across two domains 27 of life, from animals to giant bacteria.