An intranuclear bacterial parasite of deep-sea mussels expresses apoptosis inhibitors acquired from its host

Only a few bacteria are able to colonize the nuclei of eukaryotes and nearly all of these are known from protists. One bacterial clade, however, “Candidatus Endonucleobacter”, infects the nuclei of deep-sea mussels, where it replicates to ≥ 80,000 bacteria per nucleus and causes nuclei to swell to 50 times their original size. How these parasites are able to replicate so massively and avoid apoptosis is not known. Dual RNA-seq transcriptomes of infected nuclei isolated using laser-capture microdissection revealed that in contrast to previous assumptions, “Ca. Endonucleobacter” does not gain most of its nutrition from nuclear DNA or RNA. Instead, “Ca. Endonucleobacter” upregulated genes for importing sugars, lipids, amino acids and possibly mucin from its host, and digested these nutrients. “Ca. Endonucleobacter” likely prevents apoptosis of host cells by upregulating 7-13 inhibitors of apoptosis (IAPs), proteins previously only known from animals and a few invertebrate viruses. Comparative phylogenetic analyses revealed that “Ca. Endonucleobacter” acquired IAPs repeatedly through horizontal gene transfer (HGT) from their hosts in convergent acquisition. HGT from eukaryotes to bacteria, although assumed to be rare, may be more common than currently recognized, particularly in bacteria that live in intimate associations with eukaryotic hosts.