More than the “Killer Trait”: Infection with the Bacterial Endosymbiont Caedibacter taeniospiralis Causes Transcriptomic Modulation in Paramecium Host

Abstract

Endosymbiosis is a widespread phenomenon and hosts of bacterial endosymbionts can be found all-over the eukaryotic tree of life. Likely, this evolutionary success is connected to the altered phenotype arising from a symbiotic association. The potential variety of symbiont’s contributions to new characteristics or abilities of host organisms are largely unstudied. Addressing this aspect, we focused on an obligate bacterial endosymbiont that confers an intraspecific killer phenotype to its host. The symbiosis between Paramecium tetraurelia and Caedibacter taeniospiralis, living in the host’s cytoplasm, enables the infected paramecia to release Caedibacter symbionts, which can simultaneously produce a peculiar protein structure and a toxin. The ingestion of bacteria that harbor both components leads to the death of symbiont-free congeners. Thus, the symbiosis provides Caedibacter-infected cells a competitive advantage, the “killer trait.” We characterized the adaptive gene expression patterns in symbiont-harboring Paramecium as a second symbiosis-derived aspect next to the killer phenotype. Comparative transcriptomics of infected P. tetraurelia and genetically identical symbiont-free cells confirmed altered gene expression in the symbiont-bearing line. Our results show up-regulation of specific metabolic and heat shock genes whereas down-regulated genes were involved in signaling pathways and cell cycle regulation. Functional analyses to validate the transcriptomics results demonstrated that the symbiont increases host density hence providing a fitness advantage. Comparative transcriptomics shows gene expression modulation of a ciliate caused by its bacterial endosymbiont thus revealing new adaptive advantages of the symbiosis. Caedibacter taeniospiralis apparently increases its host fitness via manipulation of metabolic pathways and cell cycle control.

The Obligate Symbiont “Candidatus Megaira polyxenophila” Has Variable Effects on the Growth of Different Host Species

“…A successful treatment has been established in this study. Similar approaches for generation of the aposymbiotic lines have been used in case of other endosymbionts of Paramecium (Kusch et al, 2002;Dusi et al, 2014;Bella et al, 2016;Grosser et al, 2018). The fact that members of Rickettsiaceae are naturally resistant to a variety of antibiotics (Rolain et al, 1998) did complicate the establishment of the present protocol.…”

The concept of the hologenome, an epigenetic phenomenon, challenges aspects of the modern evolutionary synthesis

“…(d) Diversity of gene products from communities of eukaryotic excavate symbionts in termite guts reflects the environment of their host communities (Duarte, Nobre, Borges, & Nunes, 2018); (e) Hermatypic coral are dependent on the dinoflagellate Symbiodinium for 95% of their energy (Gilbert et al, 2010). (f) Acanthamoebae host amoeba-resistant bacteria like Legionella pneumophila, which have evolved to resist digestion and in some cases even to survive within human macrophages (Greub & Raoult, 2004;Loret & Greub, 2010); (g) Ciliate Paramecium tetraurelia hosts bacteria Caedibacter taeniospiralis in its cytoplasm that can kill non-host P. tetraurelia and protect current hosts from its killer mechanism (Grosser et al, 2018); (h) Single-cellular foraminifera can "steal" chloroplasts from the diatoms and other algae they eat to use for photosynthesis-a phenomenon known as kleptoplasty (Clark et al, 1990;Jauffrais et al, 2016); (i) the parasitic wasp Asobara tabida needs Wolbachia bacteria to develop into adulthood and form its ovaries properly (Gilbert et al, 2010). (j) Acrythosiphon pisum, otherwise known as pea aphids, need gene products from the endosymbiotic bacterium Buchnera aphidicola to make essential amino acids it does not get from its diet of sap (Wilson et al, 2010) bacteria in pea aphids gained a gene cluster from another endosymbiont, Cardinium or Rickettsia, through lateral gene transfer (Nikoh et al, 2014).…”

“…Host ( (2011) Amoebozoa Acanthamoeaba Diverse bacteria Greub and Raoult, (2004) and Loret and Greub, (2010) Neoparamoeba sp Perkinsela sp. (Excavata) Nowak and Archibald (2018) Rhizaria Foraminifera Dinoflagellates, diatoms Jauffrais et al (2016) and Pillet et al (2011) Alveolata Paramecium tetraurelia Caedibacter taeniospiralis Grosser et al (2018)…”

Diversity of RNA interference pathways in regulation of endogenous and exogenous sequences expression in ciliates Tetrahymena and Paramecium

“…Известно, что некодирующие РНК бактериального происхождения могут оказывать эффекты на экспрессию генов у Caenorhabditis elegans [35]. Транскриптомы P. tetraurelia, содержащих в цитоплазме симбиотические бактерии Caedibacter taeniospiralis, отличаются от транскриптомов незараженных клеток [36], а данные о появлении в клетках парамеций малых РНК, антисмысловых по отношению к транскриптам пищевых бактерий [17], позволяют допустить, что интерференция РНК может регулировать и судьбу экзогенных транскриптов, и взаимодействие инфузорий с симбионтами.…”