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Epicellular Apicomplexans: Parasites "On the Way In".

Bartošová-Sojková P, Oppenheim RD, Soldati-Favre D, Lukeš J - PLoS Pathog. (2015)

View Article: PubMed Central - PubMed

Affiliation: Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice (Budweis), Czech Republic.

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The Coccidia and the Cryptosporidia infect both cold- and warm-blooded vertebrates, yet members of the genera Toxoplasma, Eimeria, Sarcocystis, and Cryptosporidium (which mostly parasitize the latter hosts) have received most of the attention by far because of their importance to human and veterinary health... Our knowledge about a wide array of apicomplexans found in fish, amphibians, and reptiles is thus primarily confined to the morphological description of their exogenous stages (i.e., oocysts) and sites of infection, rarely with notes on pathogenicity... In the Coccidia of homeotherms, these developmental phases take place in different hosts, whereas the majority of the Coccidia of poikilotherms typically have direct life cycles... Phylogenetic analyses based on the 18S rRNA gene sequences, now available from a number of apicomplexans parasitizing cold-blooded vertebrates (e.g., members of the genera Cryptosporidium, Goussia, Acroeimeria, Eimeria, Calyptospora, and Choleoeimeria), allowed for the inference of their phylogenetic relationships... Merozoites of the epicellular species infecting fish, amphibians, and reptiles exhibit all the typical attributes of apicomplexans, yet they reside in a host-derived envelope that adopts diverse morphologies; consequently, these parasites likely rely on various modes of nutrient uptake... Importantly, an apical membrane antigen (AMA) family member and several rhoptry neck (RON) proteins discharged by the rhoptries that act as anchoring factors into the host cell cortical cytoskeleton participate in the formation of a junction through which the parasite squeezes to access the host cell... Interestingly, Cryptosporidium, which does not penetrate deeply into the host cytoplasm but remains epicellular, lacks AMAs and RONs that are necessary to form such a junction... The recently identified dense granules (GRAs) that function as effectors in subverting host cell function during Toxoplasma gondii tachyzoites infection cannot be found in G. janae... However, the aspartyl protease 5 involved in their processing and export beyond the PVM is present, which suggests that species-specific effectors likely exist in piscine coccidians... This versatility can be clearly exemplified by the metabolic flexibility of the epicellular Cryptosporidia... Indeed, intestinal human parasites Cryptosporidium parvum and C. hominis have undergone reductive evolution of their mitochondrion, leading to the loss of organellar DNA and several key functions (such as the tricarboxylic acid [TCA] cycle and respiratory chain), whereas the closely related gastric parasite of rodents, C. muris, has retained all enzymes of the TCA cycle and most complexes of the respiratory chain... The first RNA-seq analyses of the G. janae oocyst/sporozoite stages provide evidence that this coccidium possesses enzymes implicated in most of the central carbon metabolism, resembling the versatile metabolic capabilities of T. gondii rather than the reduced ones of Cryptosporidium spp. which, however, share with G. janae epicellular localization... These examples highlight potential differences in the nutrients available in each niche and specific adaptions of the parasite to thrive in its environment... In conclusion, the apicomplexans exhibit a remarkable diversity in the strategies they use for acquisition of nutrients, invasion, and interaction with host cells.

No MeSH data available.


Related in: MedlinePlus

This schematic phylogenetic tree shows the relationships among major groups of Apicomplexa and the evolution of host–parasite interactions.Phylogenetic analysis is based on the alignment of 18S rRNA gene sequences from 140 apicomplexan taxa, which were aligned in Multiple Alignment using Fast Fourier Transform (MAFFT) and analyzed using maximum likelihood criterion in RAxML, both implemented in Geneious version 8.1.3. Coccidians are monophyletic, with epicellular (EPCL) species positioned at the base of the eimeriid group and the cryptosporidia cluster within gregarines. The parasitic lifestyle likely evolved from the free-living chromerids via the myzocytic feeding of colpodellids and archigregarines. The feeding strategies of Platyproteum and Filipodium (“archigregarine” clade III) are unknown (labelled with question mark), but most likely include a kind of surface-mediated acquisition of nutrients. Neogregarines and eugregarines developed a more permanent transmembrane feeding, whereas cryptosporidians exhibit EPCL mode of nutrition using the elaborate feeder organelle. EPCL coccidians uptake nutrients through the microvillous layer of host cells. Intracellular (INCL) Apicomplexa (most eimeriid and sarcocystid coccidians, piroplasms, and haemosporidians) use both transmembrane and micropore modes of nutrient uptake. Micropores are also used for endocytosis in rhytidocystids, which are embedded in the extracellular matrix of the host’s intestinal epithelium.
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ppat.1005080.g001: This schematic phylogenetic tree shows the relationships among major groups of Apicomplexa and the evolution of host–parasite interactions.Phylogenetic analysis is based on the alignment of 18S rRNA gene sequences from 140 apicomplexan taxa, which were aligned in Multiple Alignment using Fast Fourier Transform (MAFFT) and analyzed using maximum likelihood criterion in RAxML, both implemented in Geneious version 8.1.3. Coccidians are monophyletic, with epicellular (EPCL) species positioned at the base of the eimeriid group and the cryptosporidia cluster within gregarines. The parasitic lifestyle likely evolved from the free-living chromerids via the myzocytic feeding of colpodellids and archigregarines. The feeding strategies of Platyproteum and Filipodium (“archigregarine” clade III) are unknown (labelled with question mark), but most likely include a kind of surface-mediated acquisition of nutrients. Neogregarines and eugregarines developed a more permanent transmembrane feeding, whereas cryptosporidians exhibit EPCL mode of nutrition using the elaborate feeder organelle. EPCL coccidians uptake nutrients through the microvillous layer of host cells. Intracellular (INCL) Apicomplexa (most eimeriid and sarcocystid coccidians, piroplasms, and haemosporidians) use both transmembrane and micropore modes of nutrient uptake. Micropores are also used for endocytosis in rhytidocystids, which are embedded in the extracellular matrix of the host’s intestinal epithelium.

Mentions: Phylogenetic analyses based on the 18S rRNA gene sequences, now available from a number of apicomplexans parasitizing cold-blooded vertebrates (e.g., members of the genera Cryptosporidium, Goussia, Acroeimeria, Eimeria, Calyptospora, and Choleoeimeria), allowed for the inference of their phylogenetic relationships. Piscine cryptosporidians represent a well-defined monophyletic group at the base of the cryptosporidian clade, whereas amphibian and reptile cryptosporidians are mixed with those infecting homeotherms. Coccidians of poikilotherm hosts constitute basal lineages of the whole eucoccidian clade, or of its eimeriid or sarcocystid subclades, with piscine coccidians representing the most basal groups (Fig 1) [2,3,5–7]. Because of their early-branching position, these parasites of poikilotherms likely possess ancestral features, the scrutiny of which may help us better understand the evolution of Apicomplexa. Indeed, the simple excystation structures of piscine, amphibian, and reptile coccidians have diverged into more complex excystation structures in eimeriids, sarcocystids, and calyptosporiids [2,3]. The same may apply for the site of infection, as the epicellular development seems to have been abandoned during the evolution of mammalian and avian coccidians.


Epicellular Apicomplexans: Parasites "On the Way In".

Bartošová-Sojková P, Oppenheim RD, Soldati-Favre D, Lukeš J - PLoS Pathog. (2015)

This schematic phylogenetic tree shows the relationships among major groups of Apicomplexa and the evolution of host–parasite interactions.Phylogenetic analysis is based on the alignment of 18S rRNA gene sequences from 140 apicomplexan taxa, which were aligned in Multiple Alignment using Fast Fourier Transform (MAFFT) and analyzed using maximum likelihood criterion in RAxML, both implemented in Geneious version 8.1.3. Coccidians are monophyletic, with epicellular (EPCL) species positioned at the base of the eimeriid group and the cryptosporidia cluster within gregarines. The parasitic lifestyle likely evolved from the free-living chromerids via the myzocytic feeding of colpodellids and archigregarines. The feeding strategies of Platyproteum and Filipodium (“archigregarine” clade III) are unknown (labelled with question mark), but most likely include a kind of surface-mediated acquisition of nutrients. Neogregarines and eugregarines developed a more permanent transmembrane feeding, whereas cryptosporidians exhibit EPCL mode of nutrition using the elaborate feeder organelle. EPCL coccidians uptake nutrients through the microvillous layer of host cells. Intracellular (INCL) Apicomplexa (most eimeriid and sarcocystid coccidians, piroplasms, and haemosporidians) use both transmembrane and micropore modes of nutrient uptake. Micropores are also used for endocytosis in rhytidocystids, which are embedded in the extracellular matrix of the host’s intestinal epithelium.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4581633&req=5

ppat.1005080.g001: This schematic phylogenetic tree shows the relationships among major groups of Apicomplexa and the evolution of host–parasite interactions.Phylogenetic analysis is based on the alignment of 18S rRNA gene sequences from 140 apicomplexan taxa, which were aligned in Multiple Alignment using Fast Fourier Transform (MAFFT) and analyzed using maximum likelihood criterion in RAxML, both implemented in Geneious version 8.1.3. Coccidians are monophyletic, with epicellular (EPCL) species positioned at the base of the eimeriid group and the cryptosporidia cluster within gregarines. The parasitic lifestyle likely evolved from the free-living chromerids via the myzocytic feeding of colpodellids and archigregarines. The feeding strategies of Platyproteum and Filipodium (“archigregarine” clade III) are unknown (labelled with question mark), but most likely include a kind of surface-mediated acquisition of nutrients. Neogregarines and eugregarines developed a more permanent transmembrane feeding, whereas cryptosporidians exhibit EPCL mode of nutrition using the elaborate feeder organelle. EPCL coccidians uptake nutrients through the microvillous layer of host cells. Intracellular (INCL) Apicomplexa (most eimeriid and sarcocystid coccidians, piroplasms, and haemosporidians) use both transmembrane and micropore modes of nutrient uptake. Micropores are also used for endocytosis in rhytidocystids, which are embedded in the extracellular matrix of the host’s intestinal epithelium.
Mentions: Phylogenetic analyses based on the 18S rRNA gene sequences, now available from a number of apicomplexans parasitizing cold-blooded vertebrates (e.g., members of the genera Cryptosporidium, Goussia, Acroeimeria, Eimeria, Calyptospora, and Choleoeimeria), allowed for the inference of their phylogenetic relationships. Piscine cryptosporidians represent a well-defined monophyletic group at the base of the cryptosporidian clade, whereas amphibian and reptile cryptosporidians are mixed with those infecting homeotherms. Coccidians of poikilotherm hosts constitute basal lineages of the whole eucoccidian clade, or of its eimeriid or sarcocystid subclades, with piscine coccidians representing the most basal groups (Fig 1) [2,3,5–7]. Because of their early-branching position, these parasites of poikilotherms likely possess ancestral features, the scrutiny of which may help us better understand the evolution of Apicomplexa. Indeed, the simple excystation structures of piscine, amphibian, and reptile coccidians have diverged into more complex excystation structures in eimeriids, sarcocystids, and calyptosporiids [2,3]. The same may apply for the site of infection, as the epicellular development seems to have been abandoned during the evolution of mammalian and avian coccidians.

View Article: PubMed Central - PubMed

Affiliation: Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice (Budweis), Czech Republic.

AUTOMATICALLY GENERATED EXCERPT
Please rate it.

The Coccidia and the Cryptosporidia infect both cold- and warm-blooded vertebrates, yet members of the genera Toxoplasma, Eimeria, Sarcocystis, and Cryptosporidium (which mostly parasitize the latter hosts) have received most of the attention by far because of their importance to human and veterinary health... Our knowledge about a wide array of apicomplexans found in fish, amphibians, and reptiles is thus primarily confined to the morphological description of their exogenous stages (i.e., oocysts) and sites of infection, rarely with notes on pathogenicity... In the Coccidia of homeotherms, these developmental phases take place in different hosts, whereas the majority of the Coccidia of poikilotherms typically have direct life cycles... Phylogenetic analyses based on the 18S rRNA gene sequences, now available from a number of apicomplexans parasitizing cold-blooded vertebrates (e.g., members of the genera Cryptosporidium, Goussia, Acroeimeria, Eimeria, Calyptospora, and Choleoeimeria), allowed for the inference of their phylogenetic relationships... Merozoites of the epicellular species infecting fish, amphibians, and reptiles exhibit all the typical attributes of apicomplexans, yet they reside in a host-derived envelope that adopts diverse morphologies; consequently, these parasites likely rely on various modes of nutrient uptake... Importantly, an apical membrane antigen (AMA) family member and several rhoptry neck (RON) proteins discharged by the rhoptries that act as anchoring factors into the host cell cortical cytoskeleton participate in the formation of a junction through which the parasite squeezes to access the host cell... Interestingly, Cryptosporidium, which does not penetrate deeply into the host cytoplasm but remains epicellular, lacks AMAs and RONs that are necessary to form such a junction... The recently identified dense granules (GRAs) that function as effectors in subverting host cell function during Toxoplasma gondii tachyzoites infection cannot be found in G. janae... However, the aspartyl protease 5 involved in their processing and export beyond the PVM is present, which suggests that species-specific effectors likely exist in piscine coccidians... This versatility can be clearly exemplified by the metabolic flexibility of the epicellular Cryptosporidia... Indeed, intestinal human parasites Cryptosporidium parvum and C. hominis have undergone reductive evolution of their mitochondrion, leading to the loss of organellar DNA and several key functions (such as the tricarboxylic acid [TCA] cycle and respiratory chain), whereas the closely related gastric parasite of rodents, C. muris, has retained all enzymes of the TCA cycle and most complexes of the respiratory chain... The first RNA-seq analyses of the G. janae oocyst/sporozoite stages provide evidence that this coccidium possesses enzymes implicated in most of the central carbon metabolism, resembling the versatile metabolic capabilities of T. gondii rather than the reduced ones of Cryptosporidium spp. which, however, share with G. janae epicellular localization... These examples highlight potential differences in the nutrients available in each niche and specific adaptions of the parasite to thrive in its environment... In conclusion, the apicomplexans exhibit a remarkable diversity in the strategies they use for acquisition of nutrients, invasion, and interaction with host cells.

No MeSH data available.


Related in: MedlinePlus