Regulation of host and symbiont population size inParamecium bursaria

Weis, Dale S.

doi:10.1007/bf01896584

Cited by 37 publications

(16 citation statements)

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“…The growth rate of P. bursaria cultured in this system was comparable with those reported for other systems (Fig. A, upper panel, and Table ; Siegel, ; Karakashian, ; Weis, ; Kadono et al ., ; Omura et al ., ), confirming that S. cerevisiae cells were suitable prey for P. bursaria . Neither visible cellular aggregation nor biofilm was formed in the culture at least during growth measurements, probably because of the absence of bacteria.…”

Section: Resultsmentioning

confidence: 95%

“…The population dynamics of the host P. bursaria and the endosymbiotic algae demonstrated the significant differences in their growth properties. Although growth rates were markedly different in constant darkness, they were comparable in the mid‐log phase under the normal light regime, as previously described (Weis, ). However, even under the normal light regime, the growth of the two organisms exhibited time lags, which were the main cause of the dynamic behaviours of the endosymbiont population size in the host cells.…”

Section: Resultsmentioning

confidence: 97%

“…In the log phase, the host and the endosymbiont multiplied at similar growth rates (Fig. A, upper panel, and Table ), as previously described (Weis, ). Our study, however, demonstrated that the number of endosymbionts per host was not always constant during the growth process (Fig.…”

Section: Resultsmentioning

confidence: 99%

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Maintenance of algal endosymbionts in Paramecium bursaria: a simple model based on population dynamics

Iwai

Fujiwara

Tamura

2016

Environmental Microbiology

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Algal endosymbiosis is widely distributed in eukaryotes including many protists and metazoans, and plays important roles in aquatic ecosystems, combining phagotrophy and phototrophy. To maintain a stable symbiotic relationship, endosymbiont population size in the host must be properly regulated and maintained at a constant level; however, the mechanisms underlying the maintenance of algal endosymbionts are still largely unknown. Here we investigate the population dynamics of the unicellular ciliate Paramecium bursaria and its Chlorella-like algal endosymbiont under various experimental conditions in a simple culture system. Our results suggest that endosymbiont population size in P. bursaria was not regulated by active processes such as cell division coupling between the two organisms, or partitioning of the endosymbionts at host cell division. Regardless, endosymbiont population size was eventually adjusted to a nearly constant level once cells were grown with light and nutrients. To explain this apparent regulation of population size, we propose a simple mechanism based on the different growth properties (specifically the nutrient requirements) of the two organisms, and based from this develop a mathematical model to describe the population dynamics of host and endosymbiont. The proposed mechanism and model may provide a basis for understanding the maintenance of algal endosymbionts.

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Section: Resultsmentioning

confidence: 95%

Section: Resultsmentioning

confidence: 97%

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Maintenance of algal endosymbionts in Paramecium bursaria: a simple model based on population dynamics

Iwai

Fujiwara

Tamura

2016

Environmental Microbiology

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“…Irrespective of the mutual relations between P. bursaria and symbiotic algae [7–11], the symbiont-free cells and the symbiotic algae retain the ability to grow without a partner. Symbiont-free cells can be prepared by various means: cultivation under constant dark conditions [12–14], treatment with cycloheximide [3, 15, 16], and treatment with the photosynthesis inhibitor dichlorophenyl dimethylurea (DCMU) [17]. However, symbiotic algae can be isolated by homogenization or by sonication or by the treatment of symbiotic cells with detergent.…”

Section: Introductionmentioning

confidence: 99%

Comparison of gene expression of Paramecium bursaria with and without Chlorella variabilissymbionts

et al. 2014

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BackgroundThe ciliate Paramecium bursaria harbors several hundred cells of the green-alga Chlorella sp. in their cytoplasm. Irrespective of the mutual relation between P. bursaria and the symbiotic algae, both cells retain the ability to grow without the partner. They can easily reestablish endosymbiosis when put in contact with each other. Consequently, P. bursaria is an excellent model for studying cell–cell interaction and the evolution of eukaryotic cells through secondary endosymbiosis between different protists. Despite the importance of this organism, no genomic resources have been identified for P. bursaria to date. This investigation compared gene expressions through RNA-Seq analysis and de novo transcriptome assembly of symbiont-free and symbiont-bearing host cells.ResultsTo expedite the process of gene discovery related to the endosymbiosis, we have undertaken Illumina deep sequencing of mRNAs prepared from symbiont-bearing and symbiont-free P. bursaria cells. We assembled the reads de novo to build the transcriptome. Sequencing using Illumina HiSeq2000 platform yielded 232.3 million paired-end sequence reads. Clean reads filtered from the raw reads were assembled into 68,175 contig sequences. Of these, 10,557 representative sequences were retained after removing Chlorella sequences and lowly expressed sequences. Nearly 90% of these transcript sequences were annotated by similarity search against protein databases. We identified differentially expressed genes in the symbiont-bearing P. bursaria cells relative to the symbiont-free cells, including heat shock 70 kDa protein and glutathione S-transferase.ConclusionsThis is the first reported comprehensive sequence resource of Paramecium – Chlorella endosymbiosis. Results provide some keys for the elucidation of secondary endosymbiosis in P. bursaria. We identified P. bursaria genes that are differentially expressed in symbiont-bearing and symbiont-free conditions.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-183) contains supplementary material, which is available to authorized users.

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“…These associations include various developmental stages, specifically (i) a tentative or unstable stage, we call early stage, in which partners live together during parts of life cycles depending on their ecological interactions (Reisser, 1986(Reisser, , 1993Smith & Douglas, 1987); (ii) a stable stage, in which partners live together throughout their entire life cycles and reproduce synchronously with a high rate of vertical transmission (Weis, 1969); and (iii) a genetically unified stage, often characterized by gene transfer, gene loss and/or genome reduction (McFadden, 2001). In this continuum of evolutionary stages, the early process through which unassociated organisms of different species can evolve new phenotypes to associate with each other is an important initial step.…”

Section: Introductionmentioning

confidence: 99%

Effects of acidic conditions on the physiology of a green alga (Micractiniumsp.) before and after a 5-year interaction withTetrahymena thermophilain an experimental microcosm

Germond

Inouhe

Nakajima

2014

European Journal of Phycology

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The mechanisms through which algae evolve physiological characteristics related to endosymbiotic associations with heterotrophic organisms remain unclear. We previously showed that a green alga (Micractinium sp.) was able to evolve a host (ciliate)-benefiting phenotype that prolonged the longevity of Tetrahymena thermophila in the absence of bacteria during a 5-year culture period in an experimental microcosm. Comparative experiments between the ancestral alga (i.e. original) and evolved algal clones of the same lineage can be performed to analyse the mechanisms that underlie algal evolution during interactions with ciliates. Here, we investigated the effects of acidic conditions on algal physiology because the acidic conditions within the food vacuoles of Tetrahymena could potentially affect algal evolution during long-term interactions. It might be expected that algal clones isolated from T. thermophila hosts would have developed the ability to resist acidic conditions in order to establish within the host, when compared with the ancestral strain. Unexpectedly, comparative analyses demonstrated that acidic conditions with pH values ranging from 3.9 to 4.3 limited the growth of the isolated algal clones SC9-1 and SC10-2, whereas the ancestral strain could grow under these conditions. Acidic conditions were responsible for significantly lower chlorophyll a/chlorophyll b ratios in the isolated algal clones, and the isolated clone SC9-1 exhibited a high cellular content of chlorophyllide a during a short exposure to acidic conditions, suggesting that degradation of chlorophyll a occurred. Furthermore, acidic conditions increased the release of extracellular glycerol and sucrose in the SC9-1 clone. These results indicated that the ancestral strain showed phenotypic changes related to acidic conditions, which may reflect the ongoing development of an algal phenotype suited to symbiosis. Hypotheses are proposed to explain the limited growth of the isolated clones, and implications for the Micractinium-Tetrahymena association are discussed.

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Regulation of host and symbiont population size inParamecium bursaria

Cited by 37 publications

References 0 publications

Maintenance of algal endosymbionts in Paramecium bursaria: a simple model based on population dynamics

Maintenance of algal endosymbionts in Paramecium bursaria: a simple model based on population dynamics

Comparison of gene expression of Paramecium bursaria with and without Chlorella variabilissymbionts

Effects of acidic conditions on the physiology of a green alga (Micractiniumsp.) before and after a 5-year interaction withTetrahymena thermophilain an experimental microcosm

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