Fitness Impact of Obligate Intranuclear Bacterial Symbionts Depends on Host Growth Phase

Abstract

According to text book definition, parasites reduce the fitness of their hosts whereas mutualists provide benefits. But biotic and abiotic factors influence symbiotic interactions, thus under certain circumstances parasites can provide benefits and mutualists can harm their host. Here we addressed the question which intrinsic biotic factors shape a symbiosis and are crucial for the outcome of the interaction between the obligate intranuclear bacterium Holospora caryophila (Alphaproteobacteria; Rickettsiales) and its unicellular eukaryotic host Paramecium biaurelia (Alveolata; Ciliophora). The virulence of H. caryophila, i.e., the negative fitness effect on host division and cell number, was determined by growth assays of several P. biaurelia strains. The performances of genetically identical lines either infected with H. caryophila or symbiont-free were compared. Following factors were considered as potentially influencing the outcome of the interaction: (1) host strain, (2) parasite strain, and (3) growth phases of the host. All three factors revealed a strong effect on the symbiosis. In presence of H. caryophila, the Paramecium density in the stationary growth phase decreased. Conversely, a positive effect of the bacteria during the exponential phase was observed for several host × parasite combinations resulting in an increased growth rate of infected P. biaurelia. Furthermore, the fitness impact of the tested endosymbionts on different P. biaurelia lines was not only dependent on one of the two involved strains but distinct for the specific combination. Depending on the current host growth phase, the presence of H. caryophila can be harmful or advantageous for P. biaurelia. Thus, under the tested experimental conditions, the symbionts can switch from the provision of benefits to the exploitation of host resources within the same host population and a time-span of less than 6 days.

Population‐level dynamics in experimental mixed infections: evidence for competitive exclusion among bacterial parasites of Paramecium caudatum

“…Contrary to standard assumptions of super-infection models (Nowak and May 1994), the competitive hierarchy in our system is probably not related to virulence, as the competitively superior Caryophila is less virulent than Obtusa or Undulata (Bella et al 2016) (Supplementary material Appendix 2 Fig. A4).…”

“…One possibility is that coinfection with two parasites has a strong fitness disadvantage (Griffiths et al 2011, Lass et al 2012, Susi et al 2015a, and thus doubly infected individuals may have been outcompeted by hosts harbouring single infections of Caryophila. This is conceivable, as Caryophila infection can even increase Paramecium growth rate over that of uninfected individuals (Bella et al 2016; see additional data Supplementary material Appendix 2 Fig. A4).…”

“…There was some variation in levels of persistence and prevalence in coinoculated populations due to host genotype, but no change in the rank order of infection. This may be surprising considering the large number of studies showing interactions between host and parasite genotypes, often with crossing reaction norms for infectivity and resistance related traits (Lambrechts et al 2005, de Roode and Altizer 2010), including for Paramecium-Holospora interactions (Adiba et al 2010, Duncan et al 2010, Fellous et al 2012, Bella et al 2016). Furthermore, both parasite and host genotype have been shown to change which parasite has higher fitness in a coinfection scenario (Louhi et al 2015, Klemme et al 2016, Orsucci et al 2016.…”

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

“…Reproductive forms of the bacteria (RFs) can be vertically transmitted from mother to daughter nuclei during host cell division (FUJISHIMA 2009;MAGALON et al 2010), whereas horizontal transmission occurs when infectious forms (IFs) are released during cell division or upon host death and then ingested by new hosts while feeding. Holospora symbionts show typical parasite features: they consume resources (e.g., nuclear proteins and nucleotides) in vital host compartments, disrupt sexual processes (GÖRTZ AND FUJISHIMA 1983) and reduce asexual division, cell survival, and motility (RESTIF 2006;DUNCAN et al 2010;BELLA 2016;NØRGAARD 2020;ZILIO 2020b). Several host resistance mechanisms have been described (RAUTIAN 1993;SKOBLO 1996;FOKIN 1997;FOKIN et al 2003;GOERTZ 2010); they include reduced uptake of IFs (FELS et al 2008), inability (of the bacteria) to enter the nucleus (RAUTIAN 1993) or being expelled from the nucleus after entry and before differentiating into RFs (RAUTIAN 1993;FOKIN 2005), and/or surveillance and lysis of the bacteria after it has entered and taken up residence in the nucleus (FOKIN 1997;SKOVORODKIN 2001;GOERTZ 2010).…”

Next generation taxonomy: integrating traditional species description with the holobiont concept and genomic approaches - The in-depth characterization of a novelEuplotesspecies as a case study

“…Indeed, the presence of these organisms can influence the host, its physiology, and its adaptability to the environment (e.g. Rosati et al 1999, Grosser et al, 2018, Bella et al, 2016; moreover, in some cases it has been shown to influence also its morphology (Giambelluca and Rosati 1996), the fundamental parameter of traditional taxonomy. The introduction of this novel point of view could contribute in rejuvenating the current state of taxonomy (i.e.…”