Bacterial Endocytobionts of Ciliophora and Their Interactions with the Host Cell

Fokin, Sergei I.

doi:10.1016/s0074-7696(04)36005-5

Cited by 85 publications

(105 citation statements)

References 107 publications

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“…Further, if parasites are particularly harmful, there may be selection for infected hosts to actively seek these environments [53]. Indeed, the natural distribution of Holospora species are apparently restricted to temperate regions [32]. We are currently investigating how Paramecium and their parasite populations respond to constant and variable temperature regimes lower than optimal.…”

Section: Discussionmentioning

confidence: 99%

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Temporal variation in temperature determines disease spread and maintenance inParameciummicrocosm populations

2011

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The environment is rarely constant and organisms are exposed to temporal and spatial variations that impact their life histories and inter-species interactions. It is important to understand how such variations affect epidemiological dynamics in host-parasite systems. We explored effects of temporal variation in temperature on experimental microcosm populations of the ciliate Paramecium caudatum and its bacterial parasite Holospora undulata. Infected and uninfected populations of two P. caudatum genotypes were created and four constant temperature treatments (268C, 288C, 308C and 328C) compared with four variable treatments with the same mean temperatures. Variable temperature treatments were achieved by alternating populations between permissive (238C) and restrictive (358C) conditions daily over 30 days. Variable conditions and high temperatures caused greater declines in Paramecium populations, greater fluctuations in population size and higher incidence of extinction. The additional effect of parasite infection was additive and enhanced the negative effects of the variable environment and higher temperatures by up to 50 per cent. The variable environment and high temperatures also caused a decrease in parasite prevalence (up to 40%) and an increase in extinction (absence of detection) (up to 30%). The host genotypes responded similarly to the different environmental stresses and their effect on parasite traits were generally in the same direction. This work provides, to our knowledge, the first experimental demonstration that epidemiological dynamics are influenced by environmental variation. We also emphasize the need to consider environmental variance, as well as means, when trying to understand, or predict population dynamics or range.

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Section: Discussionmentioning

confidence: 99%

“…Infection occurs through ingestion of infectious forms (15-20 mm) while feeding [32]. They are transferred to the micronucleus upon its fusion with food vesicles containing the parasite.…”

Section: Methodsmentioning

confidence: 99%

Temporal variation in temperature determines disease spread and maintenance inParameciummicrocosm populations

2011

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“…Therefore, if such symbiotic bacterial cells can be transmitted via sperm, a possible target may be the sperm head nucleus. Intranuclear bacterial symbionts, such as Holospora and Caedibacter, have been relatively well-documented from unicellular ciliates (6,15), but reported only rarely from multicellular metazoans (16,17). In insects and other arthropods, intracellular Rickettsia and Orientia pathogens/symbionts are sometimes observed to localize not only to the cytoplasm, but also to the nucleus of the host cells (18)(19)(20)(21).…”

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confidence: 99%

Intrasperm vertical symbiont transmission

Watanabe

Yukuhiro

Matsuura

et al. 2014

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

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Symbiotic bacteria are commonly associated with cells and tissues of diverse animals and other organisms, which affect hosts' biology in a variety of ways. Most of these symbionts are present in the cytoplasm of host cells and maternally transmitted through host generations. The paucity of paternal symbiont transmission is likely relevant to the extremely streamlined sperm structure: the head consisting of condensed nucleus and the tail made of microtubule bundles, without the symbiont-harboring cytoplasm that is discarded in the process of spermatogenesis. Here, we report a previously unknown mechanism of paternal symbiont transmission via an intrasperm passage. In the leafhopper Nephotettix cincticeps, a facultative Rickettsia symbiont was found not only in the cytoplasm but also in the nucleus of host cells. In male insects, strikingly, most sperm heads contained multiple intranuclear Rickettsia cells. The Rickettsia infection scarcely affected the host fitness including normal sperm functioning. Mating experiments revealed both maternal and paternal transmission of the Rickettsia symbiont through host generations. When cultured with mosquito and silkworm cell lines, the Rickettsia symbiont was preferentially localized within the insect cell nuclei, indicating that the Rickettsia symbiont itself must have a mechanism for targeting nucleus. The mechanisms underlying the sperm head infection without disturbing sperm functioning are, although currently unknown, of both basic and applied interest.

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“…Thus far, only members of the phylum Proteobacteria have been identified as intranuclear bacterial symbionts of protists and other eukaryotes (Alverca et al, 2002;Fokin, 2004;Arneodo et al, 2008;Zielinski et al, 2009). Based on their morphology, 'Candidatus Nucleococcus' (abbreviated hereafter as Nucleococcus) closely resembled Caryococcus nucleophagus, described by Kirby (1944) for the intranuclear symbionts of Trichonympha corbula, as 'Spherules with a diameter of 1/2 mm, sometimes arranged in pairs, sometimes with a thicker, crescentic, stainable area at the periphery on one side...' The genus Caryococcus was originally described for an intranuclear symbiont of the euglenid protist Euglena deses by Dangeard (1902).…”

Section: Discussionmentioning

confidence: 99%

“…Microorganisms living within the nuclei of protists were discovered in 1856 (Mü ller, 1856), and since then, numerous studies have reported both eukaryotic and prokaryotic intranuclear symbionts in diverse protist lineages (Görtz, 1986;Fokin, 2004). In the ciliates Paramecium, the macronucleus and micronucleus can be infected by specific bacterial species belonging to the genera Holospora, Caedibacter and 'Candidatus Gortzia' in the order Rickettsiales of Alphaproteobacteria (Boscaro et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Intranuclear verrucomicrobial symbionts and evidence of lateral gene transfer to the host protist in the termite gut

et al. 2013

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In 1944, Harold Kirby described microorganisms living within nuclei of the protists Trichonympha in guts of termites; however, their taxonomic assignment remains to be accomplished. Here, we identified intranuclear symbionts of Trichonympha agilis in the gut of the termite Reticulitermes speratus. We isolated single nuclei of T. agilis, performed whole-genome amplification, and obtained bacterial 16S rRNA genes by PCR. Unexpectedly, however, all of the analyzed clones were from pseudogenes of 16S rRNA with large deletions and numerous sequence variations even within a single-nucleus sample. Authentic 16S rRNA gene sequences were finally recovered by digesting the nuclear DNA; these pseudogenes were present on the host Trichonympha genome. The authentic sequences represented two distinct bacterial species belonging to the phylum Verrucomicrobia, and the pseudogenes have originated from each of the two species. Fluorescence in situ hybridization confirmed that both species are specifically localized, and occasionally co-localized, within nuclei of T. agilis. Transmission electron microscopy revealed that they are distorted cocci with characteristic electron-dense and lucent regions, which resemble the intranuclear symbionts illustrated by Kirby. For these symbionts, we propose a novel genus and species, 'Candidatus Nucleococcus trichonymphae' and 'Candidatus Nucleococcus kirbyi'. These formed a termite-specific cluster with database sequences, other members of which were also detected within nuclei of various gut protists, including both parabasalids and oxymonads. We suggest that this group is widely distributed as intranuclear symbionts of diverse protists in termite guts and that they might have affected the evolution of the host genome through lateral gene transfer.

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Bacterial Endocytobionts of Ciliophora and Their Interactions with the Host Cell

Cited by 85 publications

References 107 publications

Temporal variation in temperature determines disease spread and maintenance inParameciummicrocosm populations

Temporal variation in temperature determines disease spread and maintenance inParameciummicrocosm populations

Intrasperm vertical symbiont transmission

Intranuclear verrucomicrobial symbionts and evidence of lateral gene transfer to the host protist in the termite gut

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