Two intracellular and cell type-specific bacterial symbionts in the placozoan Trichoplax H2

Abstract

Placozoa is an enigmatic phylum of simple, microscopic, marine metazoans1,2. Although intracellular bacteria have been found in all members of this phylum, almost nothing is known about their identity, location and interactions with their host3–6. 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 parasites9,10, 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 associations11–13. 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.

Insights into the origin of metazoan multicellularity from predatory unicellular relatives of animals

“…Another noteworthy feature is the presence of symbiotic bacteria in the cells of Pigoraptor vietnamica. Symbiotic bacteria are common in both vertebrate and invertebrate animals including placozoan Trichoplax [62] and fungi [63]. Bacterial endosymbionts are also known in unicellular protists from all eukaryotic supergroups and perform a multitude of new biochemical functions in the host [64,65].…”

phyloFlash: Rapid Small-Subunit rRNA Profiling and Targeted Assembly from Metagenomes

“…This script identifies SSU rRNA sequences in the assembly, parses the assembly graph to find contigs connected to the SSU rRNA-containing contig, and optionally compares them to the SSU rRNA sequences from the initial targeted assembly from the main phyloFlash pipeline. This approach has been used to recover MAGs with SSU rRNAs from several host-associated metagenomes (46,47).…”

The diversification and lineage-specific expansion of nitric oxide signaling in Placozoa: insights in the evolution of gaseous transmission

“…This hypothesis is consistent with our present finding of the micromolar concentration of nitrites in Trichoplax . Because many placozoan cells (e.g., fiber cells) do contain endosymbiotic bacteria 79 , 80 , additional levels of intra- and intercellular NO-dependent communications are also highly likely and can be tested in future studies. Nevertheless, we do not expect that endosymbiotic bacteria produce NO and therefore cross-react with our microchemical/pharmacological assays.…”

“…2 , some bacteria do contain animal-like NOS genes, the sequenced genomes of placozoan endosymbionts 79 , 80 do not encode any recognizable NOS. Moreover, the estimated volume/mass occupied by endosymbionts is substantially less than these parameters in Trichoplax cells 79 .…”