Forced symbiosis between<i>Synechocystis</i>spp. PCC 6803 and apo-symbiotic<i>Paramecium bursaria</i>as an experimental model for evolutionary emergence of primitive photosynthetic eukaryotes

Ohkawa, Hiroshi; Hashimoto, Naoko; Furukawa, Shunsuke; Kadono, Takashi; Kawano, Tomonori

doi:10.4161/psb.6.6.15239

Cited by 17 publications

(12 citation statements)

References 21 publications

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“…The approach has also been used to investigate obligate associations. Advances in culturing and experimental methodologies have allowed the transfer of obligate endosymbiotic Buchnera strains into new aphid matrilines (Moran and Yun 2015), and the replacement of the endogenous eukaryotic alga with a novel cyanobacterial partner in Paramecium bursaria (Ohkawa et al 2011). Similar approaches can even establish symbionts in entirely novel hosts, such as the permanent lines of vertically inherited Wolbachia strains in novel Aedes mosquito hosts (Walker et al 2011).…”

Section: Co-culturesmentioning

confidence: 99%

Co-cultures of Oophila amblystomatis between Ambystoma maculatum and Ambystoma gracile hosts show host-symbiont fidelity

et al. 2019

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A unique symbiosis occurs between embryos of the spotted salamander (Ambystoma maculatum) and a green alga (Oophila amblystomatis). Unlike most vertebrate host-symbiont relationships, which are ectosymbiotic, A. maculatum exhibits both an ecto-and an endo-symbiosis, where some of the green algal cells living inside egg capsules enter embryonic tissues as well as individual salamander cells. Past research has consistently categorized this symbiosis as a mutualism, making this the first example of a Bbeneficial^microbe entering vertebrate cells. Another closely related species of salamander, Ambystoma gracile, also harbors beneficial Oophila algae in its egg capsules. However, our sampling within the A. gracile range consistently shows this to be a strict ectosymbiotic interaction-with no sign of tissue or presumably cellular entry. In this study we swapped cultured algae derived from intracapsular fluid of different salamander hosts to test the fidelity of tissue entry in these symbioses. Both A. maculatum and A. gracile embryos were raised in cultures with their own algae or algae cultured from the other host. Under these in vitro culture conditions A. maculatum algae will enter embryonic A. maculatum tissues. Additionally, although at a much lower frequency, A. gracile derived algae will also enter A. maculatum host tissues. However, neither Oophila strain enters A. gracile hosts in these co-culture conditions. These data reveal a potential host-symbiont fidelity that allows the unique endosymbiosis to occur in A. maculatum, but not in A. gracile. However, preliminary trials in our study found that persistent endogenous A. maculatum algae, as opposed to the cultured algae used in subsequent trials, enters host tissues at a higher frequency. An analysis of previously published Oophila transcriptomes revealed dramatic differences in gene expression between cultured and intracapsular Oophila. These include a suite of genes in protein and cell wall synthesis, photosynthesis, central carbon metabolism suggesting the intracapsular algae are assimilating ammonia for nitrogen metabolism and may be undergoing a life-cycle transition. Further refinements of these coculture conditions could help determine physiological differences between cultured and endogenous algae, as well as rate-limiting cues provided for the alga by the salamander.

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Section: Co-culturesmentioning

confidence: 99%

Co-cultures of Oophila amblystomatis between Ambystoma maculatum and Ambystoma gracile hosts show host-symbiont fidelity

et al. 2019

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“…Recently, an artificial endosymbiosis was created by supplying aposymbiotic Paramecium bursaria with Synechocystis PCC6803 [ 13 ]. These organisms do not naturally form a symbiosis and so have not coevolved.…”

Section: Introductionmentioning

confidence: 99%

“…The interchange of metabolites between host and symbiont is key to understanding the evolutionary mechanisms for symbiosis formation. The metabolic exchange between the ciliate and Synechocystis in the novel interaction reported by Ohkawa et al [ 13 ] is unlikely to be identical to that between P. bursaria and Chlorella , because the maltose exporter is an Archaeplastida innovation and there is no evidence to suggest Synechocystis can produce maltose [ 24 , 25 ]. The exchanges, however, are probably similar, because Paramecium 's recognition of potential symbionts will most likely require a supply of certain metabolites.…”

Section: Introductionmentioning

confidence: 99%

Metabolic constraints for a novel symbiosis

et al. 2016

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Ancient evolutionary events are difficult to study because their current products are derived forms altered by millions of years of adaptation. The primary endosymbiotic event formed the first photosynthetic eukaryote resulting in both plants and algae, with vast consequences for life on Earth. The evolutionary time that passed since this event means the dominant mechanisms and changes that were required are obscured. Synthetic symbioses such as the novel interaction between Paramecium bursaria and the cyanobacterium Synechocystis PC6803, recently established in the laboratory, permit a unique window on the possible early trajectories of this critical evolutionary event. Here, we apply metabolic modelling, using flux balance analysis (FBA), to predict the metabolic adaptations necessary for this previously free-living symbiont to transition to the endosymbiotic niche. By enforcing reciprocal nutrient trading, we are able to predict the most efficient exchange nutrients for both host and symbiont. During the transition from free-living to obligate symbiosis, it is likely that the trading parameters will change over time, which leads in our model to discontinuous changes in the preferred exchange nutrients. Our results show the applicability of FBA modelling to ancient evolutionary transitions driven by metabolic exchanges, and predict how newly established endosymbioses, governed by conflict, will differ from a well-developed one that has reached a mutual-benefit state.

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“…(12,13) Instead of inert particles, several living organisms such as photosynthetic bacteria (a strain derived from Synechocystis sp. PCC 6803) (14,15) or nonsymbiotic algae (16) can also be introduced. Thus, this organism provides a highly advanced model for evolutionary emergence of photosynthetic organisms through the development of symbiosis.…”

Section: Introductionmentioning

confidence: 99%

“…3. (a) Cyanobacteria (PCC 6803)-loaded cells of P. bursaria prepared according to the method of Ohkawa et al(14) (b) Distribution of cells in the capillary before application of electric stimulus. (c) 10 min after static incubation without electric stimulus.…”

mentioning

confidence: 99%

Enhanced Microsphere Transport in Capillary by Conditioned Cells of Green Paramecia Used as Living Micromachines Controlled by Electric Stimuli

Furukawa¹,

Kawano

2012

Sensors and Materials

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Some researchers have described the cells of Paramecium species as "swimming sensory cells" or "swimming neurons" applicable to micro-biorobotics and biological micro-electromechanical systems (BioMEMS). Paramecium species including green paramecia (Paramecium bursaria) migrate towards the anodic electrode when exposed to an electric field. This type of cellular movement is known as galvanotaxis. Because the ideal micromachines designed for microparticle transport must have a capacity for loading certain numbers of particles, P. bursaria was chosen as a model organism. In this study, we show enhanced microparticle transport by overcoming (i) the particle size limitation for the cell-mediated transport of microspheres of up to ca. 10 µm size (doubling the size of particles ever reported) and (ii) the limit of cellular migration distance manifested by galvanotactically stimulated cells.

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Forced symbiosis betweenSynechocystisspp. PCC 6803 and apo-symbioticParamecium bursariaas an experimental model for evolutionary emergence of primitive photosynthetic eukaryotes

Cited by 17 publications

References 21 publications

Co-cultures of Oophila amblystomatis between Ambystoma maculatum and Ambystoma gracile hosts show host-symbiont fidelity

Co-cultures of Oophila amblystomatis between Ambystoma maculatum and Ambystoma gracile hosts show host-symbiont fidelity

Metabolic constraints for a novel symbiosis

Enhanced Microsphere Transport in Capillary by Conditioned Cells of Green Paramecia Used as Living Micromachines Controlled by Electric Stimuli

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