Feeding exogenous dsRNA interferes with endogenous sRNA accumulation in<i>Paramecium</i>

Karunanithi, Sivarajan; Oruganti, Vidya; Wijn, Raphaël de; Drews, Franziska; Cheaib, Miriam; Nordström, Karl; Simón, Martín; Schulz, Marcel H.

doi:10.1093/dnares/dsaa005

Cited by 4 publications

(3 citation statements)

References 39 publications

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“…Paramecium can also process single-stranded RNA (ssRNA)—including ribosomal RNA (rRNA) and messenger RNA (mRNA)—derived from a prokaryotic cell acquired through phagotrophy ( 43 , 48 ). This processing is mediated by conserved RNAi protein components, many of which also function in endogenous transcriptome regulation ( 42 , 43 , 45 , 48 , 49 ). Significantly, these studies propose that mRNA, derived both exogenously ( 42 , 43 ) and endogenously ( 42 , 45 ), can act as substrates for siRNA generation in Paramecium .…”

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confidence: 99%

Emergent RNA–RNA interactions can promote stability in a facultative phototrophic endosymbiosis

Jenkins

Maguire

Leonard

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Eukaryote–eukaryote endosymbiosis was responsible for the spread of chloroplast (plastid) organelles. Stability is required for the metabolic and genetic integration that drives the establishment of new organelles, yet the mechanisms that act to stabilize emergent endosymbioses—between two fundamentally selfish biological organisms—are unclear. Theory suggests that enforcement mechanisms, which punish misbehavior, may act to stabilize such interactions by resolving conflict. However, how such mechanisms can emerge in a facultative endosymbiosis has yet to be explored. Here, we propose that endosymbiont–host RNA–RNA interactions, arising from digestion of the endosymbiont population, can result in a cost to host growth for breakdown of the endosymbiosis. Using the model facultative endosymbiosis between Paramecium bursaria and Chlorella spp., we demonstrate that this mechanism is dependent on the host RNA-interference (RNAi) system. We reveal through small RNA (sRNA) sequencing that endosymbiont-derived messenger RNA (mRNA) released upon endosymbiont digestion can be processed by the host RNAi system into 23-nt sRNA. We predict multiple regions of shared sequence identity between endosymbiont and host mRNA, and demonstrate through delivery of synthetic endosymbiont sRNA that exposure to these regions can knock down expression of complementary host genes, resulting in a cost to host growth. This process of host gene knockdown in response to endosymbiont-derived RNA processing by host RNAi factors, which we term “RNAi collisions,” represents a mechanism that can promote stability in a facultative eukaryote–eukaryote endosymbiosis. Specifically, by imposing a cost for breakdown of the endosymbiosis, endosymbiont–host RNA–RNA interactions may drive maintenance of the symbiosis across fluctuating ecological conditions.

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mentioning

confidence: 99%

Emergent RNA–RNA interactions can promote stability in a facultative phototrophic endosymbiosis

Jenkins

Maguire

Leonard

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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“…In nematodes, for instance, viral RNAs are 3′-uridinylated as part of a conserved antiviral mechanism (Le Pen et al, 2018). However, this is unlikely, as both RDRs involved in the feeding mechanisms are also necessary for a certain number of endogenous siRNA clusters, so there seems to be a mechanistic overlap between exogenous and endogenous RNAi (Karunanithi et al, 2019(Karunanithi et al, , 2020.…”

Section: Primary and Secondary Sirnas Are Involved In Feeding Induced...mentioning

confidence: 99%

Paramecium epigenetics in development and proliferation

Drews

Boenigk

Simón

2022

J Eukaryotic Microbiology

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CILIATES, particularly Paramecium, served as model organisms in genetics and epigenetics long before the latter term was even used for the first time. From the historical point of view, ciliate genetics had its first's heydays from 1940 to 1960, when many important discoveries were made, resulting in a detailed description of epigenetic phenomena. As a result, most textbooks for undergraduates dedicated individual chapters to ciliate cell biology and genetics in the 1970s, but these chapters disappeared from textbooks in modern times (Preer, 1997).This situation has now changed (Boenigk, 2021). Ciliate epigenetic research experiences a renaissance, although this wording might not be entirely precise as research is not simply making a replica of the former work. We are now able to describe epigenetic phenomena discovered phenotypically in the early 1940s on the molecular level and identify small RNAs, histone modifications, and DNA modifications that are responsible for these phenomena. Still, genetics research is primarily based on yeast, C. elegans, Drosophila, zebrafish, and

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“…Paramecium can also process single-stranded RNA (ssRNA) – including ribosomal RNA (rRNA) and messenger RNA (mRNA) – derived from a prokaryotic cell acquired through phagotrophy 42 . This processing is mediated by conserved RNAi protein components which also function in endogenous transcriptome regulation 41,42,44,47 . Significantly, these studies propose that mRNA, derived both exogenously 41,42 and endogenously 41,44 , can act as substrates for siRNA generation in Paramecium .…”

Section: Main Textmentioning

confidence: 99%

Emergent RNA-RNA interactions can promote stability in a nascent phototrophic endosymbiosis

Jenkins

Maguire

Leonard

et al. 2021

Preprint

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Eukaryote-eukaryote endosymbiosis was responsible for the spread of photosynthetic organelles. Interaction stability is required for the metabolic and genetic integration that drives the establishment of new organelles, yet the mechanisms which act to stabilise nascent endosymbioses - between two fundamentally selfish biological organisms - are unclear. Theory suggests that enforcement mechanisms, which punish misbehaviour, may act to stabilise such interactions by resolving conflict. However, how such mechanisms can emerge in a nascent eukaryote-eukaryote endosymbiosis has yet to be explored. Here, we propose that endosymbiont-host RNA-RNA interactions, arising from digestion of endosymbionts, can result in a cost to host growth for breakdown of the endosymbiosis. Using the model nascent endosymbiosis, Paramecium bursaria - Chlorella spp., we demonstrate that this mechanism is dependent on the host RNA-interference (RNAi) pathway. We reveal through small RNA (sRNA) sequencing that endosymbiont-derived mRNA released upon endosymbiont digestion can be processed by the host RNAi system into 23-nt sRNA. We additionally identify multiple regions of shared sequence identity between endosymbiont and host mRNA, and demonstrate, through delivery of synthetic endosymbiont sRNA, that exposure to these regions can knock-down expression of complementary host genes, resulting in a cost to host growth. This process of host gene knock-down in response to endosymbiont-derived RNA processing by the host, which we term 'RNAi-collisions', represents a mechanism which can promote stability in a nascent eukaryote-eukaryote endosymbiosis. By imposing a cost for breakdown of the endosymbiosis, endosymbiont-host RNA-RNA interactions may drive maintenance of a symbiosis across fluctuating ecologies and symbiotic states.

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Feeding exogenous dsRNA interferes with endogenous sRNA accumulation inParamecium

Cited by 4 publications

References 39 publications

Emergent RNA–RNA interactions can promote stability in a facultative phototrophic endosymbiosis

Emergent RNA–RNA interactions can promote stability in a facultative phototrophic endosymbiosis

Paramecium epigenetics in development and proliferation

Emergent RNA-RNA interactions can promote stability in a nascent phototrophic endosymbiosis

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