Natural distribution and co-infection patterns of microsporidia parasites in the<i>Daphnia longispina</i>complex

Microsporidia are a group of obligate intracellular parasites that are best known for their unique infection mechanism and their unparalleled levels of genomic reduction and compaction. We sequenced the genome of Ordospora colligata, a gut parasite of the microcrustacean Daphnia sp. and the closest known relative to the microsporidia characterized by the most extreme genomic reduction, the model genus Encephalitozoon. We found that the O. colligata genome is as compact as those of Encephalitozoon spp., featuring few introns and a similar complement of about 2,000 genes, altogether showing that the extreme reduction took place before the origin of Encephalitozoon spp. and their adaptation to vertebrate hosts. We also found that the O. colligata genome has acquired by horizontal transfer from its animal host a septin that is structurally analogous to septin 7, a protein that plays a major role in the endocytosis-based invasion mechanism of the fungal pathogen Candida albicans. Microsporidian invasion is most often characterized by injection through a projectile tube, but microsporidia are also known to invade cells by inducing endocytosis. Given the function of septins in other systems, we hypothesize that the acquired septin could help O. colligata induce its uptake by mimicking host receptors.Importance The smallest known eukaryotic genomes are found in members of the Encephalitozoon genus of microsporidian parasites. Their extreme compaction, however, is not characteristic of the group, whose genomes can differ by an order of magnitude. The processes and evolutionary forces that led the Encephalitozoon genomes to shed so much of their ancestral baggage are unclear. We sequenced the genome of Ordospora colligata, a parasite of the water flea Daphnia sp. and the closest known relative of Encephalitozoon species, and show that this extreme reduction predated the split between the two lineages. We also found that O. colligata has acquired a septin gene by host-to-parasite horizontal transfer and predicted that the encoded protein folds like a septin 7, which plays a major role in endocytosis. We hypothesize that this acquisition could help O. colligata parasitize its hosts by facilitating endocytic infection, a mechanism that occurs in microsporidia but that is not yet well understood.

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“… Daphnia spp. are susceptible to many microsporidian species, which are widespread across the phylogenetic tree ( 17 , 20 , 21 ).…”

Section: Resultsmentioning

confidence: 99%

The Ordospora colligata Genome: Evolution of Extreme Reduction in Microsporidia and Host-To-Parasite Horizontal Gene Transfer

Pombert

Haag

Beidas

et al. 2015

mBio

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“…Hence, PCR assays with specific markers such as those developed in this and other studies (e.g. Hogg et al 2002;Weigl et al 2012) remain the most accurate method to reliably detect microsporidian infections and to accurately estimate their prevalence in the field. In addition, these molecular techniques allow morphologically similar species to be distinguished within 3-6 days of hosts being infected.…”

Section: Detection Of Cryptic Infectionmentioning

confidence: 94%

Cytological, molecular and life cycle characterization of Anostracospora rigaudi n. g., n. sp. and Enterocytospora artemiae n. g., n. sp., two new microsporidian parasites infecting gut tissues of the brine shrimp Artemia

et al. 2013

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Two new microsporidia, Anostracospora rigaudi n. g., n. sp., and Enterocytospora artemiae n. g., n. sp. infecting the intestinal epithelium of Artemia parthenogenetica Bowen and Sterling, 1978 and Artemia franciscana Kellogg, 1906 in southern France are described. Molecular analyses revealed the two species belong to a clade of microsporidian parasites that preferentially infect the intestinal epithelium of insect and crustacean hosts. These parasites are morphologically distinguishable from other gut microsporidia infecting Artemia. All life cycle stages have isolated nuclei. Fixed spores measure 1·3×0·7 μm with 5-6 polar tube coils for A. rigaudi and 1·2×0·9 μm with 4 polar tube coils for E. artemiae. Transmission of both species is horizontal, most likely through the ingestion of spores released with the faeces of infected hosts. The minute size of these species, together with their intestinal localization, makes their detection and identification difficult. We developed two species-specific molecular markers allowing each type of infection to be detected within 3-6 days post-inoculation. Using these markers, we show that the prevalence of these microsporidia ranges from 20% to 75% in natural populations. Hence, this study illustrates the usefulness of molecular approaches to study prevalent, but cryptic, infections involving microsporidian parasites of gut tissues.

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“…[ 26 , 27 ]). In addition, microsporidian parasites of Daphnia have received considerable attention due to their complex life-cycles [ 28 – 30 ]. In our study, we focused on two abundant microsporidians infecting Daphnia communities inhabiting large lakes and reservoirs in central Europe, classified as Berwaldia schaefernai and as the microsporidium MIC1 [ 31 ].…”

Section: Introductionmentioning

confidence: 99%

“…Both of these species infect the body cavity of their host, where a massive amount of spores then proliferate [ 32 ]. They are closely related to Marssoniella elegans (a parasite of the copepod Cyclops vicinus ), Senoma globulifera (a parasite of the malaria-hosting mosquito Anopheles messeae ), and other parasites of Daphnia , including Larssonia obtusa , Gurleya vavrai and Binucleata daphniae [ 30 ]; these relatives span a range of transmission and reproduction modes. Marssoniella elegans is a dixenous parasite which likely uses mosquitoes or caddisflies as secondary hosts [ 33 , 34 ], while S. globulifera and B. daphniae are monoxenous parasites [ 29 , 35 ].…”

Section: Introductionmentioning

confidence: 99%

Genetic diversity of two Daphnia-infecting microsporidian parasites, based on sequence variation in the internal transcribed spacer region

et al. 2016

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BackgroundMicrosporidia are spore-forming obligate intracellular parasites that include both emerging pathogens and economically important disease agents. However, little is known about the genetic diversity of microsporidia. Here, we investigated patterns of geographic population structure, intraspecific genetic variation, and recombination in two microsporidian taxa that commonly infect cladocerans of the Daphnia longispina complex in central Europe. Taken together, this information helps elucidate the reproductive mode and life-cycles of these parasite species.MethodsMicrosporidia-infected Daphnia were sampled from seven drinking water reservoirs in the Czech Republic. Two microsporidia species (Berwaldia schaefernai and microsporidium lineage MIC1) were sequenced at the internal transcribed spacer (ITS) region, using the 454 pyrosequencing platform. Geographical structure analyses were performed applying Fisher’s exact tests, analyses of molecular variance, and permutational MANOVA. To evaluate the genetic diversity of the ITS region, the number of polymorphic sites and Tajima’s and Watterson’s estimators of theta were calculated. Tajima’s D was also used to determine if the ITS in these taxa evolved neutrally. Finally, neighbour similarity score and pairwise homology index tests were performed to detect recombination events.ResultsWhile there was little variation among Berwaldia parasite strains infecting different host populations, the among-population genetic variation of MIC1 was significant. Likewise, ITS genetic diversity was lower in Berwaldia than in MIC1. Recombination signals were detected only in Berwaldia.ConclusionGenetic tests showed that parasite populations could have expanded recently after a bottleneck or that the ITS could be under negative selection in both microsporidia species. Recombination analyses might indicate cryptic sex in Berwaldia and pure asexuality in MIC1. The differences observed between the two microsporidian species present an exciting opportunity to study the genetic basis of microsporidia-Daphnia coevolution in natural populations, and to better understand reproduction in these parasites.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-016-1584-4) contains supplementary material, which is available to authorized users.

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Natural distribution and co-infection patterns of microsporidia parasites in theDaphnia longispinacomplex

Cited by 16 publications

References 60 publications

The Ordospora colligata Genome: Evolution of Extreme Reduction in Microsporidia and Host-To-Parasite Horizontal Gene Transfer

The Ordospora colligata Genome: Evolution of Extreme Reduction in Microsporidia and Host-To-Parasite Horizontal Gene Transfer

Cytological, molecular and life cycle characterization of Anostracospora rigaudi n. g., n. sp. and Enterocytospora artemiae n. g., n. sp., two new microsporidian parasites infecting gut tissues of the brine shrimp Artemia

Genetic diversity of two Daphnia-infecting microsporidian parasites, based on sequence variation in the internal transcribed spacer region

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