The formation of the Paramecium-Holospora symbiotic system: a study of the compatibility of different symbiont isolates and host clones

Skoblo, I. I.; Lebedeva, N. A.; Rodionova, Galina V.

doi:10.1016/s0932-4739(96)80092-7

Cited by 8 publications

(13 citation statements)

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“…Yet, the strains that we used in our analysis come from many different geographical regions (Table S1), and there might be some aspects that we are unaware of, that cause some strains to be less subject to the effect of parasite infection on dispersal. Seminal work on our Paramecium-Holospora system illustrated the presence of different compatibilities between parasite isolate and host clones (Skoblo et al, 1996), and the potential for variation and evolution of resistance. Still, as mentioned before, explanation different from an adaptive perspective might apply.…”

Section: Is Plasticity Selected For?mentioning

confidence: 99%

Parasitism and host dispersal plasticity in an aquatic model system

Zilio

Nørgaard

Petrucci

et al. 2020

Preprint

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Dispersal plays a main role in determining spatial dynamics, and both theory and empirical evidence indicate that evolutionary optima exist for constitutive or plastic dispersal behaviour. Plasticity in dispersal can be influenced by factors both internal (state-dependent) or external (context-dependent) to individuals. Parasitism is interesting in this context, as it can influence both types of host dispersal plasticity: individuals can disperse in response to internal infection status but might also respond to the presence of infected individuals around them. We still know little about the driving evolutionary forces of host dispersal plasticity, but a first requirement is the presence of a genetic basis on which natural selection can act. In this study, we used microcosm dispersal mazes to investigate plastic dispersal of 20 strains of the freshwater protist Paramecium caudatum in response to the bacterial parasite Holospora undulata. We additionally quantified the genetic component of the plastic responses, i.e. the heritability of state- and context-depended dispersal. We found that infection by the parasite can either increase or decrease dispersal of individual strains relative to the uninfected (state-dependent plasticity), and this to be heritable. We also found strain-specific change of dispersal of uninfected Paramecium when exposed to variable infection prevalence (context-dependent plasticity) with very low level of heritability. To our knowledge, this is the first explicit empirical demonstration and quantification of genetic variation of plastic dispersal in a host-parasite system, which could have important implications for meta-population and epidemiological dynamics. We discuss some of the underlying mechanisms of this variation and link our results to the existing theoretical models.

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Section: Is Plasticity Selected For?mentioning

confidence: 99%

Parasitism and host dispersal plasticity in an aquatic model system

Zilio

Nørgaard

Petrucci

et al. 2020

Preprint

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“…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).…”

Section: Introductionmentioning

confidence: 99%

“…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'.…”

Section: Introductionmentioning

confidence: 99%

“…Given the strong species-specificity of Holospora, such cryptic species complexes may represent an important structural component of resistance variation in natural populations. Indeed, Fujishima and Fujita (1985) found that Holospora obtusa was only able to infect strains from 5 out of 6 of the P. caudatum syngens studied, whereas an extensive study on Holospora undulata revealed successful infection of 84 of 92 P. caudatum strains and all 10 syngens tested (SKOBLO 1996). In yet another system, Rautian et al (1993) reported evidence of strong syngen-level specificity of strains from Holospora acuminata on Paramecium bursaria, and this across a wide range of geographic origins.…”

Section: Introductionmentioning

confidence: 99%

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

Weiler

Zilio

Zeballos

et al. 2020

Preprint

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Resistance is a key determinant in interactions between hosts and their parasites. Understanding the amount and distribution of genetic variation in this trait can provide insights into (co)evolutionary processes and their potential to shape patterns of diversity in natural populations. Using controlled inoculation in experimental mass cultures, we investigated the quantitative genetic variation in resistance to the bacterial parasite Holospora undulata across a worldwide collection of strains of its ciliate host Paramecium caudatum. We combined the observed variation with available information on the phylogeny and biogeography of the strains. We found substantial variation in resistance among strains (with broad-sense heritability > 0.5), repeatable between laboratories and ranging from total resistance to near-complete susceptibility. Early (one week post inoculation) measurements provided higher estimates of resistance heritability than did later measurements (2-3 weeks), possibly due to diverging epidemiological dynamics in replicate cultures of the same strains. Genetic distance (based on a neutral marker) was positively correlated with the difference in resistance phenotype between strains (r = 0.45), essentially reflecting differences between highly divergent clades (haplogroups) within the host species. Haplogroup A strains, mostly European, were less resistant to the parasite (49% infection prevalence) than non-European haplogroup B strains (28%). At a smaller geographical scale (within Europe), strains that are geographically closer to the parasite origin (Southern Germany) were more susceptible to infection than those from further away. These patterns are consistent with a picture of local parasite adaptation. Our study demonstrates ample natural genetic variation in resistance on which selection can act and hints at symbiont adaptation producing signatures in geographic and lineage-specific patterns of resistance in this model system.

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“…The second half of the 1980s, and especially the 1990s and the beginning of the 2000s was the time of the most intensive scientific activity of Hans-Dieter and his colleagues in the field of symbiontology (Görtz, 1983(Görtz, , 1986(Görtz, , 1987(Görtz, , 1988(Görtz, , 1996(Görtz, , 1998(Görtz, , 2008(Görtz, , 2010(Görtz, , 2014Görtz and Wiemann, 1989;Fujishima et al, 1990Fujishima et al, , 1991Fujishima et al, , 1997Heckmann and Görtz, 1991;Fokin and Skovorodkin, 1991a, 1991bFokin, 1993;2004a;Ossipov et al, 1993;Fokin et al, 1996Fokin et al, , 2003bFokin et al, , 2005Fokin et al, , 2006Skoblo et al, 1996;Görtz and Brigge, 1998;Görtz et al, 1990Görtz et al, , 1993Görtz et al, , 2009Skovorodkin et al, 2001;Görtz and Michel, 2003;Nakamura et al, 2004;Görtz and Schmidt, 2005;Iwatani et al, 2005;Lang et al, 2005;Sabaneyeva et al, 2005Sabaneyeva et al, , 2007Schrallhammer at al., 2006;Fema et al, 2008;Görtz and Fokin, 2009;Fokin and Görtz, 2009;Schrallhammer and Schweikert, 2009, and many others). A number of his students have ...…”

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confidence: 99%

Professor Hans-Dieter Görtz (1945–2019). In memory of my close friend and colleague

Fokin¹

2019

Protistology

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The formation of the Paramecium-Holospora symbiotic system: a study of the compatibility of different symbiont isolates and host clones

Cited by 8 publications

References 4 publications

Parasitism and host dispersal plasticity in an aquatic model system

Parasitism and host dispersal plasticity in an aquatic model system

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

Professor Hans-Dieter Görtz (1945–2019). In memory of my close friend and colleague

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