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Abstract

Placozoa is an enigmatic phylum of simple, microscopic, marine
metazoans(1,2). Although intracellular bacteria have been found in all
members of this phylum, almost nothing is known about their identity,
location and interactions with their host(3-6). We used metagenomic and
metatranscriptomic sequencing of single host individuals, plus
metaproteomic and imaging analyses, to show that the placozoan
Trichoplax sp. H2 lives in symbiosis with two intracellular bacteria.
One symbiont forms an undescribed genus in the Midichloriaceae
(Rickettsiales)(7,8) and has a genomic repertoire similar to that of
rickettsial parasites(9,10), but does not seem to express key genes for
energy parasitism. Correlative image analyses and three-dimensional
electron tomography revealed that this symbiont resides in the rough
endoplasmic reticulum of its host's internal fibre cells. The second
symbiont belongs to the Margulisbacteria, a phylum without cultured
representatives and not known to form intracellular associations(11-13).
This symbiont lives in the ventral epithelial cells of Trichoplax,
probably metabolizes algal lipids digested by its host and has the
capacity to supplement the placozoan's nutrition. Our study shows that
one of the simplest animals has evolved highly specific and intimate
associations with symbiotic, intracellular bacteria and highlights that
symbioses can provide access to otherwise elusive microbial dark matter.