Genome analyses of a placozoan rickettsial endosymbiont show a combination of mutualistic and parasitic traits

Abstract

Symbiotic relationships between eukaryotic hosts and bacteria range from parasitism to mutualism and may deeply influence both partners’ fitness. The presence of intracellular bacteria in the metazoan phylum Placozoa has been reported several times, but without any knowledge about the nature of this relationship and possible implications for the placozoan holobiont. This information may be of crucial significance since little is known about placozoan ecology and how different species adapt to different environmental conditions, despite being almost invariable at the morphological level. We here report on the novel genome of the rickettsial endosymbiont of Trichoplax sp. H2 (strain “Panama”). The combination of eliminated and retained metabolic pathways of the bacterium indicates a potential for a mutualistic as well as for a parasitic relationship, whose outcome could depend on the environmental context. In particular we show that the endosymbiont is dependent on the host for growth and reproduction and that the latter could benefit from a supply with essential amino acids and important cofactors. These findings call for further studies to clarify the actual benefit for the placozoan host and to investigate a possible role of the endosymbiont for ecological separation between placozoan species.

Evolution ofWolbachiamutualism and reproductive parasitism: insight from two novel strains that co-infect cat fleas

“…Order Rickettsiales is a highly diverse group of obligate intracellular bacteria ( Gillespie et al, 2012 ; Driscoll et al, 2013 ; Darby et al, 2007 ). A rapid pace of newly identified lineages ( Klinges et al, 2019 ; Castelli et al, 2019 ; Tashyreva et al, 2018 ; Kamm et al, 2019 ; Gruber-Vodicka et al, 2019 ; Martijn et al, 2015 ; Schulz et al, 2016 ; Yurchenko et al, 2018 ; Schrallhammer et al, 2013 ; Montagna et al, 2013 ; Boscaro et al, 2019 ; Muñoz-Gómez et al, 2019 ; Mediannikov et al, 2014 ; Szokoli et al, 2016 ; Prokopchuk et al, 2019 ) provides a rich source for evaluating mechanisms of evolution within constraints of the eukaryotic cell. Phage, plasmids, transposons, ICEs, and other insertion sequences are variably present across rickettsial genomes and mobilize numerous genes to offset reductive genome evolution and provide lifestyle altering traits ( Gillespie et al, 2012 ).…”

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

“…Although, as we showed in Fig. 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 .…”

“…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.…”

“…Trichoplax contains intracellular bacteria, which present only in a specific and relatively small population of cells—primarily, the fiber cells 79 , 80 . Potentially, these bacteria could contribute to enzymatic NO production and interfere with obtained measurements of NOS related metabolites.…”

“…Potentially, these bacteria could contribute to enzymatic NO production and interfere with obtained measurements of NOS related metabolites. The genomes of two bacterial endosymbionts ( Grellia incantans (Midichloriaceae/Rickettsiales) and Ruthmannia eludens (Margulisbacteria) in H2 have been recently sequenced 79 , 80 , but they do not contain recognizable NOSs. Thus, it is highly unlikely that NO in Trichoplax can be produced by bacteria.…”