Towards an ecological understanding of the killer trait – A reproducible protocol for testing its impact on freshwater ciliates

Koehler, Lars; Flemming, Felicitas E.; Schrallhammer, Martina

doi:10.1016/j.ejop.2019.02.002

Cited by 3 publications

(7 citation statements)

References 44 publications

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“…Killer test assays were performed as described previously (Koehler et al, 2019 ). In brief, R-body production by the bacterial endosymbionts was promoted by not feeding the paramecia for at least 7 days.…”

Section: Methodsmentioning

confidence: 99%

“…As they require resources from the host cell, these bacteria inflict costs on Paramecium (Dusi et al, 2014 ; Weiler et al, 2020 ) like reduction in cell division, motility, survival (Restif and Kaltz, 2006 ; Nørgaard et al, 2021 ; Zilio et al, 2020 ) as well as the potential disruption of sexual processes (Görtz and Fujishima, 1983 ). On the other hand, several experimental studies show that paramecia carrying a bacterial endosymbiont have an advantage relative to aposymbiotic or symbiont-free cells (Hori and Fujishima, 2003 ; Bella et al, 2016 ; Grosser et al, 2018 ; Schu and Schrallhammer, 2018 ; Koehler et al, 2019 ; Pasqualetti et al, 2020 ). In the following, the term aposymbiotic is used to describe cells which have lost their endosymbionts, e.g., by antibiotic treatment, hence, these aposymbiotic cells once harbored a bacterial infection which was subsequently eliminated.…”

Section: Introductionmentioning

confidence: 99%

“…Another advantageous trait provided by bacterial endosymbionts to Paramecium is the so-called killer trait (Schrallhammer et al, 2012 ; Koehler et al, 2019 ). Bacteria belonging to the genera Caedibacter and Caedimonas (Schrallhammer et al, 2018 ) provide their hosts with a complex strategy to outcompete congeners not harboring the respective bacterial symbiont (Schrallhammer et al, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

“…Bacteria belonging to the genera Caedibacter and Caedimonas (Schrallhammer et al, 2018 ) provide their hosts with a complex strategy to outcompete congeners not harboring the respective bacterial symbiont (Schrallhammer et al, 2018 ). Refractile bodies (R-bodies) produced by the endosymbionts act as delivery system for an unidentified toxin which causes the death of sensitive, aposymbiotic, or symbiont-free paramecia after ingestion (Schrallhammer et al, 2012 ; Koehler et al, 2019 ).…”

Section: Introductionmentioning

confidence: 99%

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Natural Shifts in Endosymbionts' Occurrence and Relative Frequency in Their Ciliate Host Population

2022

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The role of bacterial endosymbionts harbored by heterotrophic Paramecium species is complex. Obligate intracellular bacteria supposedly always inflict costs as the host is the only possible provider of resources. However, several experimental studies have shown that paramecia carrying bacterial endosymbionts can benefit from their infection. Here, we address the question which endosymbionts occur in natural paramecia populations isolated from a small lake over a period of 5 years and which factors might explain observed shifts and persistence in the symbionts occurrence. One hundred and nineteen monoclonal strains were investigated and approximately two-third harbored intracellular bacteria. The majority of infected paramecia carried the obligate endosymbiotic “Candidatus Megaira polyxenophila”, followed by Caedimonas varicaedens, and Holospora undulata. The latter was only detected in a single strain. While “Ca. M. polyxenophila” was observed in seven out of 13 samplings, C. varicaedens presence was limited to a single sampling occasion. After the appearance of C. varicaedens, “Ca. M. polyxenophila” prevalence dramatically dropped with some delay but recovered to original levels at the end of our study. Potential mechanisms explaining these observations include differences in infectivity, host range, and impact on host fitness as well as host competitive capacities. Growth experiments revealed fitness advantages for infected paramecia harboring “Ca. M. polyxenophila” as well as C. varicaedens. Furthermore, we showed that cells carrying C. varicaedens gain a competitive advantage from the symbiosis-derived killer trait. Other characteristics like infectivity and overlapping host range were taken into consideration, but the observed temporal persistence of “Ca. M. polyxenophila” is most likely explained by the positive effect this symbiont provides to its host.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Natural Shifts in Endosymbionts' Occurrence and Relative Frequency in Their Ciliate Host Population

2022

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“…This ciliate is studied, among other things ( Karunanithi et al, 2019 ; Kelz and Mashour, 2019 ; Mayne et al, 2019 ; Soares et al, 2019 ; Arnaiz et al, 2020 ) for the abundance and diversity of its endosymbionts ( Floriano et al, 2018 ; Garushyants et al, 2018 ; Grosser et al, 2018 ; Potekhin et al, 2018 ; Sabaneyeva et al, 2018 ; Schrallhammer et al, 2018 ; Castelli et al, 2019a , b ; Fokin et al, 2019 ; Koehler et al, 2019 ; Lanzoni et al, 2019 ; Plotnikov et al, 2019 ). Host-symbiont interactions and their outcome have been studied for example using Holospora ( Lohse et al, 2006 ; Hori et al, 2008 ; Fokin and Görtz, 2009 ; Nidelet et al, 2009 ; Duncan et al, 2013 , 2018 ; Banerji et al, 2015 ; Castelli et al, 2015 ; Dusi et al, 2015 ; Garushyants et al, 2018 ; Grosser et al, 2018 ) Caedibacter ( Kusch et al, 2002 ; Dusi et al, 2014 ; Grosser et al, 2018 ; Schu and Schrallhammer, 2018 ; Koehler et al, 2019 ) and Preeria ( Bella et al, 2016 ; Potekhin et al, 2018 ). Despite an increasing number of studies, our knowledge about the impact of symbionts on Paramecium is limited, especially when considering that this ciliate is among the best studied protists in regard to host-symbiont interactions.…”

Section: Introductionmentioning

confidence: 99%

The Obligate Symbiont “Candidatus Megaira polyxenophila” Has Variable Effects on the Growth of Different Host Species

et al. 2020

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Candidatus Megaira polyxenophila" is a recently described member of Rickettsiaceae which comprises exclusively obligate intracellular bacteria. Interestingly, these bacteria can be found in a huge diversity of eukaryotic hosts (protist, green algae, metazoa) living in marine, brackish or freshwater habitats. Screening of amplicon datasets revealed a high frequency of these bacteria especially in freshwater environments, most likely associated to eukaryotic hosts. The relationship of "Ca. Megaira polyxenophila" with their hosts and their impact on host fitness have not been studied so far. Even less is known regarding the responses of these intracellular bacteria to potential stressors. In this study, we used two phylogenetically close species of the freshwater ciliate Paramecium, Paramecium primaurelia and Paramecium pentaurelia (Ciliophora, Oligohymenophorea) naturally infected by "Ca. Megaira polyxenophila". In order to analyze the effect of the symbiont on the fitness of these two species, we compared the growth performance of both infected and aposymbiotic paramecia at different salinity levels in the range of freshwater and oligohaline brackish water i.e., at 0, 2, and 4.5 ppt. For the elimination of "Ca. Megaira polyxenophila" we established an antibiotic treatment to obtain symbiont-free lines and confirmed its success by fluorescence in situ hybridization (FISH). The population and infection dynamics during the growth experiment were observed by cell density counts and FISH. Paramecia fitness was compared applying generalized additive mixed models. Surprisingly, both infected Paramecium species showed higher densities under all salinity concentrations. The tested salinity concentrations did not significantly affect the growth of any of the two species directly, but we observed the loss of the endosymbiont after prolonged exposure to higher salinity levels. This experimental data might explain the higher frequency of "Ca. M. polyxenophila" in freshwater habitats as observed from amplicon data.

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

Pirritano

Zaburannyi

Grosser

et al. 2020

Sci Rep

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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.

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Towards an ecological understanding of the killer trait – A reproducible protocol for testing its impact on freshwater ciliates

Cited by 3 publications

References 44 publications

Natural Shifts in Endosymbionts' Occurrence and Relative Frequency in Their Ciliate Host Population

Natural Shifts in Endosymbionts' Occurrence and Relative Frequency in Their Ciliate Host Population

The Obligate Symbiont “Candidatus Megaira polyxenophila” Has Variable Effects on the Growth of Different Host Species

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

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