Bacterial symbiosis in ciliates (Alveolata, Ciliophora): Roads traveled and those still to be taken

Abstract

The diversity of prokaryotic symbionts in Ciliophora and other protists is fascinatingly rich; they may even include some potentially pathogenic bacteria. In this review, we summarize currently available data on biodiversity and some morphological and biological peculiarities of prokaryotic symbionts mainly within the genera Paramecium and Euplotes. Another direction of ciliate symbiology, neglected for a long time and now re-discovered, is the study of epibionts of ciliates. This promises a variety of interesting outcomes. Last, but not least, we stress the new technologies, such as next generation sequencing and the use of genomics data, which all can clarify many new aspects of relevance. For this reason, a brief overview of achievements in genomic studies on ciliate's symbionts is provided. Summing up the results of numerous scientific contributions, we systematically update current knowledge and outline the prospects as to how symbiology of Ciliophora may develop in the near future.

Keywords: Euplotes; Holospora; Paramecium; Ciliophora; Holospora-like bacteria; endosymbiosis; episymbiosis; morphology; phylogeny; symbionts.

FIGURE 1

Morphology of Holospora and Holospora‐like bacteria. (A) Equatorial connecting piece (CP) of a dividing Paramecium caudatum macronucleus infected with H. obtusa. (B) Macronucleus of P. putrinum infected with “Ca. Gortzia yakutica” undergoing division shows the absence of the CP (asterisk). (C) Ultrastructure of the infectious form (IF) of “Ca. Holospora parva”; recognition tip (T); the arrowhead indicates the subdivision of periplasmic space (P); bacterial cytoplasm (C). (D) “Ca. Gortzia infectiva” reproductive form (RF), other abbreviations are the same. (E) IF and RF of Preeria caryophila. IF with two recognition tips, located at the opposite ends of the bacterial cell. (F) IF of “Ca. Gortzia shahrazadis”. All abbreviations are the same as in (C–E). (A, B) differential interference contrast microscopy; (C–F) transmission electron microscopy. Scale bars represent 20 μm (A), 10 μm (B), 0.3 μm (C), 1.0 μm (D), 0.6 μm (E), 0.5 μm (F)

FIGURE 2

Bayesian inference tree of the family Holosporaceae based on 16S rRNA gene sequences (1288 character matrix). Numbers on nodes represent posterior probabilities and maximum likelihood bootstrap values, respectively (only values above 0.85–75 are shown). Bar stands for an estimated sequence divergence of 9%