Complex life cycle, broad host range and adaptation strategy of the intranuclear Paramecium symbiont Preeria caryophila comb. nov

Abstract

Holospora and related bacteria are a group of obligate Paramecium symbionts. Characteristic features are their infectivity, the presence of two distinct morphotypes, and usually a strict specialization for a single Paramecium species as host and for a nuclear compartment (either somatic or generative nucleus) for reproduction. Holospora caryophila steps out of line, naturally occurring in Paramecium biaurelia and Paramecium caudatum. This study addresses the phylogenetic relationship among H. caryophila and other Holospora species based on 16S rRNA gene sequence comparison analyzing the type strain and seven new macronuclear symbionts. Key aspects of Holospora physiology such as infectivity, symbiosis establishment and host range were determined by comprehensive infection assays. Detailed morphological investigations and sequence-based phylogeny confirmed a high similarity between the type strain of H. caryophila and the novel strains. Surprisingly, they are only distantly related to other Holospora species suggesting that they belong to a new genus within the family Holosporaceae, here described as Preeria caryophila comb. nov. Adding to this phylogenetic distance, we also observed a much broader host range, comprising at least eleven Paramecium species. As these potential host species exhibit substantial differences in frequency of sexual processes, P. caryophila demonstrates which adaptations are crucial for macronuclear symbionts facing regular destruction of their habitat.

Heritable variation in resistance to the endonuclear parasiteHolospora undulataacross clades ofParamecium caudatum

“…Another potential mechanism contributing to the maintenance of genetic diversity is genotypespecific adaptation, or more generally, host genotype x parasite genotype interactions (LAMBRECHTS et al 2005; CAYETANO AND VORBURGER 2013). Previous work indicated large-scale differences in qualitative resistance between entire syngens, or mating groups, within Paramecium species (FUJISHIMA AND FUJITA 1985;RAUTIAN 1993;SKOBLO 1996;POTEKHIN et al 2018). This might reflect signatures of lineage-specific adaptation, such that certain groups of Holospora strains can only infect certain Paramecium syngens (RAUTIAN 1993).…”

“…The infection life cycle (Figure 1) is well-characterized for different Holospora species (GÖRTZ 1980;FUJISHIMA 2009;POTEKHIN et al 2018). All species show the same morphological and functional dimorphism, with infectious forms (IFs; elongated, up to µm) and reproductive forms (RFs; more rounded, oblong, 5 µm).…”

“…as Rickettsia or Wolbachia (SZOKOLI et al 2016;GARUSHYANTS et al 2018;POTEKHIN et al 2018;MUNOZ-GOMEZ et al 2019). Following the discovery of Holospora bacteria in the 19th century (HAFKINE 1890), there has been extensive research on their morphology, infection life cycle, and taxonomic relationships (for a historical overview, see ).…”

“…Holospora species infect one single host species, and only the phylogenetically more distant Holospora caryophila (now Ca. Preeria caryophila) is known to occur on multiple host species (POTEKHIN et al 2018). Furthermore, the interaction is obligate for the bacterium, and replication is only possible inside the host cell, as many biosynthetic metabolic pathways are fractured or even missing GARUSHYANTS et al 2018).…”

“…Holospora have been found at low infection prevalences in temperate or elevated locations around the globe (FOKIN 1993;HORI AND FUJISHIMA 2003;FOKIN et al 2004;SERRA et al 2016), but can occasionally cause local epidemics , which might give a strong selective advantage to resistant variants over susceptible ones. Previous cross-inoculation studies demonstrated the existence of such natural variation, showing that different strains of Paramecium caudatum (and several other species) have different qualitative infection phenotypes, with some strains appearing universally susceptible to infection with Holospora, while others are more difficult to infect or even entirely resistant (FUJISHIMA AND FUJITA 1985;RAUTIAN 1993;RAUTIAN 1996;SKOBLO 1996;POTEKHIN et al 2018). Previous studies have also compared resistance across independent mating groups or 'syngens'.…”