Dual-Seq reveals genome and transcriptome of Caedibacter taeniospiralis, obligate endosymbiont of Paramecium

Abstract

Interest in host-symbiont interactions is continuously increasing, not only due to the growing recognition of the importance of microbiomes. Starting with the detection and description of novel symbionts, attention moves to the molecular consequences and innovations of symbioses. However, molecular analysis requires genomic data which is difficult to obtain from obligate intracellular and uncultivated bacteria. We report the identification of the Caedibacter genome, an obligate symbiont of the ciliate Paramecium. The infection does not only confer the host with the ability to kill other cells but also renders them immune against this effect. We obtained the C. taeniospiralis genome and transcriptome by dual-Seq of DNA and RNA from infected paramecia. Comparison of codon usage and expression level indicates that genes necessary for a specific trait of this symbiosis, i.e. the delivery of an unknown toxin, result from horizontal gene transfer hinting to the relevance of DNA transfer for acquiring new characters. Prediction of secreted proteins of Caedibacter as major agents of contact with the host implies, next to several toxin candidates, a rather uncharacterized secretome which appears to be highly adapted to this symbiosis. Our data provides new insights into the molecular establishment and evolution of this obligate symbiosis and for the pathway characterization of toxicity and immunity.

‘Candidatus Sarmatiella mevalonica’ endosymbiont of the ciliate Paramecium provides insights on evolutionary plasticity among Rickettsiales

“…We predict that deep genomic analyses from such novel and/or neglected lineages, as in case of Sarmatiella and several recent others (Sassera et al ., 2011; Mediannikov et al ., 2014; Pilgrim et al ., 2017), in particular those associated with aquatic hosts (Schulz et al ., 2016; Floriano et al ., 2018; Yurchenko et al ., 2018; Gruber‐Vodicka et al ., 2019; Klinges et al ., 2019; Castelli et al ., 2019a; George et al ., 2020), will offer a wider comparative perspective, for a better reconstruction of the evolutionary paths of Rickettsiales and the underlying genomic processes. Additionally, a better understanding of their interaction with the hosts, including through transcriptome analyses (see as examples Yang et al ., 2016; Gruber‐Vodicka et al ., 2019; Pirritano et al ., 2020; Midha et al ., 2020), may significantly contribute as well, providing validated functional grounds for comparative and evolutionary inferences.…”

Identification of novel, functional, long noncoding RNAs involved in programmed, large-scale genome rearrangements

“…Ribosomal RNA was depleted using the Ribo-Zero Gold rRNA Removal Kit (yeast; Illumina) following the manufacturer's protocol. This kit has been previously used for studies conducted in Paramecium ( Gotz et al 2016 ; Pirritano et al 2020 ). In order to eliminate the majority of mRNA transcripts, we performed poly(A) depletion using the Dynabeads mRNA Purification Kit (Invitrogen, Thermo Fisher Scientific).…”

Epigenetic influences of mobile genetic elements on ciliate genome architecture and evolution

“…This capability is conferred by Caedibacter endosymbionts, specifically, those possessing an organelle called an R‐body that is thought to release the toxin (Grosser et al, 2018; Pond et al, 1989; Preer & Jurand, 1968; Preer & Preer, 1967; Schrallhammer et al, 2012). Observations of phage‐like particles near R‐bodies, and more recent genomic and transcriptomic sequencing of a Caedibacter species, indicate that genes encoding the R‐body may be derived from bacteriophages (Pirritano et al, 2020; Pond et al, 1989). In this case, the bacterium serves as a necessary intermediate for viral‐derived elements to express a trait that enhances ciliate fitness.…”