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Article ; Online: Advances in Understanding Leishmania Pathobiology

Tamara Salloum / Sima Tokajian / Robert P. Hirt

Frontiers in Cell and Developmental Biology, Vol

What Does RNA-Seq Tell Us?

2021 Volume 9

Abstract: Leishmaniasis is a vector-borne disease caused by a protozoa parasite from over 20 Leishmania species. The clinical manifestations and the outcome of the disease vary greatly. Global RNA sequencing (RNA-Seq) analyses emerged as a powerful technique to ... ...

Abstract	Leishmaniasis is a vector-borne disease caused by a protozoa parasite from over 20 Leishmania species. The clinical manifestations and the outcome of the disease vary greatly. Global RNA sequencing (RNA-Seq) analyses emerged as a powerful technique to profile the changes in the transcriptome that occur in the Leishmania parasites and their infected host cells as the parasites progresses through their life cycle. Following the bite of a sandfly vector, Leishmania are transmitted to a mammalian host where neutrophils and macrophages are key cells mediating the interactions with the parasites and result in either the elimination the infection or contributing to its proliferation. This review focuses on RNA-Seq based transcriptomics analyses and summarizes the main findings derived from this technology. In doing so, we will highlight caveats in our understanding of the parasite’s pathobiology and suggest novel directions for research, including integrating more recent data highlighting the role of the bacterial members of the sandfly gut microbiota and the mammalian host skin microbiota in their potential role in influencing the quantitative and qualitative aspects of leishmaniasis pathology.
Keywords	Leishmania ; RNA-Seq ; gene expression ; promastigotes ; amastigotes ; macrophages ; Biology (General) ; QH301-705.5
Subject code	630
Language	English
Publishing date	2021-09-01T00:00:00Z
Publisher	Frontiers Media S.A.
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Microsporidia

Paul Dean / Robert P Hirt / T Martin Embley

PLoS Pathogens, Vol 12, Iss 11, p e

Why Make Nucleotides if You Can Steal Them?

2016 Volume 1005870

Abstract: Microsporidia are strict obligate intracellular parasites that infect a wide range of eukaryotes including humans and economically important fish and insects. Surviving and flourishing inside another eukaryotic cell is a very specialised lifestyle that ... ...

Abstract	Microsporidia are strict obligate intracellular parasites that infect a wide range of eukaryotes including humans and economically important fish and insects. Surviving and flourishing inside another eukaryotic cell is a very specialised lifestyle that requires evolutionary innovation. Genome sequence analyses show that microsporidia have lost most of the genes needed for making primary metabolites, such as amino acids and nucleotides, and also that they have only a limited capacity for making adenosine triphosphate (ATP). Since microsporidia cannot grow and replicate without the enormous amounts of energy and nucleotide building blocks needed for protein, DNA, and RNA biosynthesis, they must have evolved ways of stealing these substrates from the infected host cell. Providing they can do this, genome analyses suggest that microsporidia have the enzyme repertoire needed to use and regenerate the imported nucleotides efficiently. Recent functional studies suggest that a critical innovation for adapting to intracellular life was the acquisition by lateral gene transfer of nucleotide transport (NTT) proteins that are now present in multiple copies in all microsporidian genomes. These proteins are expressed on the parasite surface and allow microsporidia to steal ATP and other purine nucleotides for energy and biosynthesis from their host. However, it remains unclear how other essential metabolites, such as pyrimidine nucleotides, are acquired. Transcriptomic and experimental studies suggest that microsporidia might manipulate host cell metabolism and cell biological processes to promote nucleotide synthesis and to maximise the potential for ATP and nucleotide import. In this review, we summarise recent genomic and functional data relating to how microsporidia exploit their hosts for energy and building blocks needed for growth and nucleic acid metabolism and we identify some remaining outstanding questions.
Keywords	Immunologic diseases. Allergy ; RC581-607 ; Biology (General) ; QH301-705.5
Subject code	612 ; 572
Language	English
Publishing date	2016-11-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Adaptation to genome decay in the structure of the smallest eukaryotic ribosome

David Nicholson / Marco Salamina / Johan Panek / Karla Helena-Bueno / Charlotte R. Brown / Robert P. Hirt / Neil A. Ranson / Sergey V. Melnikov

Nature Communications, Vol 13, Iss 1, Pp 1-

2022 Volume 12

Abstract: Many parasitic organisms contain molecular structures that are drastically smaller than analogous structures in non-parasitic organisms. Here the authors describe a cryo-EM structure of the ribosome from E. cuniculi that reveals that it compensated rRNA ... ...

Abstract	Many parasitic organisms contain molecular structures that are drastically smaller than analogous structures in non-parasitic organisms. Here the authors describe a cryo-EM structure of the ribosome from E. cuniculi that reveals that it compensated rRNA truncations by evolving the ability to use small molecules as ribosomal building blocks.
Keywords	Science ; Q
Language	English
Publishing date	2022-02-01T00:00:00Z
Publisher	Nature Portfolio
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Expanded genome-wide comparisons give novel insights into population structure and genetic heterogeneity of Leishmania tropica complex.

Tamara Salloum / Rim Moussa / Ryan Rahy / Jospin Al Deek / Ibrahim Khalifeh / Rana El Hajj / Neil Hall / Robert P Hirt / Sima Tokajian

PLoS Neglected Tropical Diseases, Vol 14, Iss 9, p e

2020 Volume 0008684

Abstract: Leishmania tropica is one of the main causative agents of cutaneous leishmaniasis (CL). Population structures of L. tropica appear to be genetically highly diverse. However, the relationship between L. tropica strains genomic diversity, protein coding ... ...

Abstract	Leishmania tropica is one of the main causative agents of cutaneous leishmaniasis (CL). Population structures of L. tropica appear to be genetically highly diverse. However, the relationship between L. tropica strains genomic diversity, protein coding gene evolution and biogeography are still poorly understood. In this study, we sequenced the genomes of three new clinical L. tropica isolates, two derived from a recent outbreak of CL in camps hosting Syrian refugees in Lebanon and one historical isolate from Azerbaijan to further refine comparative genome analyses. In silico multilocus microsatellite typing (MLMT) was performed to integrate the current diversity of genome sequence data in the wider available MLMT genetic population framework. Single nucleotide polymorphism (SNPs), gene copy number variations (CNVs) and chromosome ploidy were investigated across the available 18 L. tropica genomes with a main focus on protein coding genes. MLMT divided the strains in three populations that broadly correlated with their geographical distribution but not populations defined by SNPs. Unique SNPs profiles divided the 18 strains into five populations based on principal component analysis. Gene ontology enrichment analysis of the protein coding genes with population specific SNPs profiles revealed various biological processes, including iron acquisition, sterols synthesis and drug resistance. This study further highlights the complex links between L. tropica important genomic heterogeneity and the parasite broad geographic distribution. Unique sequence features in protein coding genes identified in distinct populations reveal potential novel markers that could be exploited for the development of more accurate typing schemes to further improve our knowledge of the evolution and epidemiology of the parasite as well as highlighting protein variants of potential functional importance underlying L. tropica specific biology.
Keywords	Arctic medicine. Tropical medicine ; RC955-962 ; Public aspects of medicine ; RA1-1270
Subject code	572
Language	English
Publishing date	2020-09-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: A new family of cell surface located purine transporters in Microsporidia and related fungal endoparasites

Peter Major / Kacper M Sendra / Paul Dean / Tom A Williams / Andrew K Watson / David T Thwaites / T Martin Embley / Robert P Hirt

eLife, Vol

2019 Volume 8

Abstract: Plasma membrane-located transport proteins are key adaptations for obligate intracellular Microsporidia parasites, because they can use them to steal host metabolites the parasites need to grow and replicate. However, despite their importance, the ... ...

Abstract	Plasma membrane-located transport proteins are key adaptations for obligate intracellular Microsporidia parasites, because they can use them to steal host metabolites the parasites need to grow and replicate. However, despite their importance, the functions and substrate specificities of most Microsporidia transporters are unknown. Here, we provide functional data for a family of transporters conserved in all microsporidian genomes and also in the genomes of related endoparasites. The universal retention among otherwise highly reduced genomes indicates an important role for these transporters for intracellular parasites. Using Trachipleistophora hominis, a Microsporidia isolated from an HIV/AIDS patient, as our experimental model, we show that the proteins are ATP and GTP transporters located on the surface of parasites during their intracellular growth and replication. Our work identifies a new route for the acquisition of essential energy and nucleotides for a major group of intracellular parasites that infect most animal species including humans.
Keywords	Microsporidia ; Trachipleistophora hominis ; rabbit cell line RK13 ; Rozellomycota ; nucleotide parasitism ; Medicine ; R ; Science ; Q ; Biology (General) ; QH301-705.5
Subject code	572
Language	English
Publishing date	2019-07-01T00:00:00Z
Publisher	eLife Sciences Publications Ltd
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: A metazoan/plant-like capping enzyme and cap modified nucleotides in the unicellular eukaryote Trichomonas vaginalis.

Augusto Simoes-Barbosa / Robert P Hirt / Patricia J Johnson

PLoS Pathogens, Vol 6, Iss 7, p e

2010 Volume 1000999

Abstract: The cap structure of eukaryotic messenger RNAs is initially elaborated through three enzymatic reactions: hydrolysis of the 5'-triphosphate, transfer of guanosine through a 5'-5' triphosphate linkage and N7-methylation of the guanine cap. Three ... ...

Abstract	The cap structure of eukaryotic messenger RNAs is initially elaborated through three enzymatic reactions: hydrolysis of the 5'-triphosphate, transfer of guanosine through a 5'-5' triphosphate linkage and N7-methylation of the guanine cap. Three distinctive enzymes catalyze each reaction in various microbial eukaryotes, whereas the first two enzymes are fused into a single polypeptide in metazoans and plants. In addition to the guanosine cap, adjacent nucleotides are 2'-O-ribose methylated in metazoa and plants, but not in yeast. Analyses of various cap structures have suggested a linear phylogenetic trend of complexity. These findings have led to a model in which plants and metazoa evolved a two-component capping apparatus and modification of adjacent nucleotides while many microbial eukaryotes maintained the three-component system and did not develop modification of adjacent nucleotides. Here, we have characterized a bifunctional capping enzyme in the divergent microbial eukaryote Trichomonas vaginalis using biochemical and phylogenetic analyses. This unicellular parasite was found to harbor a metazoan/plant-like capping apparatus that is represented by a two-domain polypeptide containing a C-terminus guanylyltransferase and a cysteinyl phosphatase triphosphatase, distinct from its counterpart in other microbial eukaryotes. In addition, T. vaginalis mRNAs contain a cap 1 structure represented by m(7)GpppAmpUp or m(7)GpppCmpUp; a feature typical of metazoan and plant mRNAs but absent in yeast mRNAs. Phylogenetic and biochemical analyses of the origin of the T. vaginalis capping enzyme suggests a complex evolutionary model where differential gene loss and/or acquisition occurred in the development of the RNA capping apparatus and cap modified nucleotides during eukaryote diversification.
Keywords	Immunologic diseases. Allergy ; RC581-607 ; Biology (General) ; QH301-705.5
Subject code	580
Language	English
Publishing date	2010-07-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: A novel extracellular metallopeptidase domain shared by animal host-associated mutualistic and pathogenic microbes.

Sirintra Nakjang / Didier A Ndeh / Anil Wipat / David N Bolam / Robert P Hirt

PLoS ONE, Vol 7, Iss 1, p e

2012 Volume 30287

Abstract: The mucosal microbiota is recognised as an important factor for our health, with many disease states linked to imbalances in the normal community structure. Hence, there is considerable interest in identifying the molecular basis of human-microbe ... ...

Abstract	The mucosal microbiota is recognised as an important factor for our health, with many disease states linked to imbalances in the normal community structure. Hence, there is considerable interest in identifying the molecular basis of human-microbe interactions. In this work we investigated the capacity of microbes to thrive on mucosal surfaces, either as mutualists, commensals or pathogens, using comparative genomics to identify co-occurring molecular traits. We identified a novel domain we named M60-like/PF13402 (new Pfam entry PF13402), which was detected mainly among proteins from animal host mucosa-associated prokaryotic and eukaryotic microbes ranging from mutualists to pathogens. Lateral gene transfers between distantly related microbes explained their shared M60-like/PF13402 domain. The novel domain is characterised by a zinc-metallopeptidase-like motif and is distantly related to known viral enhancin zinc-metallopeptidases. Signal peptides and/or cell surface anchoring features were detected in most microbial M60-like/PF13402 domain-containing proteins, indicating that these proteins target an extracellular substrate. A significant subset of these putative peptidases was further characterised by the presence of associated domains belonging to carbohydrate-binding module family 5/12, 32 and 51 and other glycan-binding domains, suggesting that these novel proteases are targeted to complex glycoproteins such as mucins. An in vitro mucinase assay demonstrated degradation of mammalian mucins by a recombinant form of an M60-like/PF13402-containing protein from the gut mutualist Bacteroides thetaiotaomicron. This study reveals that M60-like domains are peptidases targeting host glycoproteins. These peptidases likely play an important role in successful colonisation of both vertebrate mucosal surfaces and the invertebrate digestive tract by both mutualistic and pathogenic microbes. Moreover, 141 entries across various peptidase families described in the MEROPS database were also identified with ...
Keywords	Medicine ; R ; Science ; Q
Subject code	572
Language	English
Publishing date	2012-01-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Evolutionary conservation and in vitro reconstitution of microsporidian iron–sulfur cluster biosynthesis

Sven-A. Freibert / Alina V. Goldberg / Christian Hacker / Sabine Molik / Paul Dean / Tom A. Williams / Sirintra Nakjang / Shaojun Long / Kacper Sendra / Eckhard Bill / Eva Heinz / Robert P. Hirt / John M Lucocq / T. Martin Embley / Roland Lill

Nature Communications, Vol 8, Iss 1, Pp 1-

2017 Volume 12

Abstract: The functions of the highly reduced mitochondria (mitosomes) of microsporidians are not well-characterized. Here, the authors show that theTrachipleistophora hominismitosome is the site of iron–sulfur cluster assembly and that its retention is likely ... ...

Abstract	The functions of the highly reduced mitochondria (mitosomes) of microsporidians are not well-characterized. Here, the authors show that theTrachipleistophora hominismitosome is the site of iron–sulfur cluster assembly and that its retention is likely linked to its role in cytosolic and nuclear iron–sulfur protein maturation.
Keywords	Science ; Q
Language	English
Publishing date	2017-01-01T00:00:00Z
Publisher	Nature Portfolio
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Plasma membrane-located purine nucleotide transport proteins are key components for host exploitation by microsporidian intracellular parasites.

Eva Heinz / Christian Hacker / Paul Dean / John Mifsud / Alina V Goldberg / Tom A Williams / Sirintra Nakjang / Alison Gregory / Robert P Hirt / John M Lucocq / Edmund R S Kunji / T Martin Embley

PLoS Pathogens, Vol 10, Iss 12, p e

2014 Volume 1004547

Abstract: Microsporidia are obligate intracellular parasites of most animal groups including humans, but despite their significant economic and medical importance there are major gaps in our understanding of how they exploit infected host cells. We have ... ...

Abstract	Microsporidia are obligate intracellular parasites of most animal groups including humans, but despite their significant economic and medical importance there are major gaps in our understanding of how they exploit infected host cells. We have investigated the evolution, cellular locations and substrate specificities of a family of nucleotide transport (NTT) proteins from Trachipleistophora hominis, a microsporidian isolated from an HIV/AIDS patient. Transport proteins are critical to microsporidian success because they compensate for the dramatic loss of metabolic pathways that is a hallmark of the group. Our data demonstrate that the use of plasma membrane-located nucleotide transport proteins (NTT) is a key strategy adopted by microsporidians to exploit host cells. Acquisition of an ancestral transporter gene at the base of the microsporidian radiation was followed by lineage-specific events of gene duplication, which in the case of T. hominis has generated four paralogous NTT transporters. All four T. hominis NTT proteins are located predominantly to the plasma membrane of replicating intracellular cells where they can mediate transport at the host-parasite interface. In contrast to published data for Encephalitozoon cuniculi, we found no evidence for the location for any of the T. hominis NTT transporters to its minimal mitochondria (mitosomes), consistent with lineage-specific differences in transporter and mitosome evolution. All of the T. hominis NTTs transported radiolabelled purine nucleotides (ATP, ADP, GTP and GDP) when expressed in Escherichia coli, but did not transport radiolabelled pyrimidine nucleotides. Genome analysis suggests that imported purine nucleotides could be used by T. hominis to make all of the critical purine-based building-blocks for DNA and RNA biosynthesis during parasite intracellular replication, as well as providing essential energy for parasite cellular metabolism and protein synthesis.
Keywords	Immunologic diseases. Allergy ; RC581-607 ; Biology (General) ; QH301-705.5
Subject code	572
Language	English
Publishing date	2014-12-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article: Reduction and Expansion in Microsporidian Genome Evolution: New Insights from Comparative Genomics

Nakjang, Sirintra / Tom A. Williams / Eva Heinz / Andrew K. Watson / Peter G. Foster / Kacper M. Sendra / Sarah E. Heaps / Robert P. Hirt / T. Martin Embley

Genome biology and evolution. 2013, v. 5, no. 12

2013

Abstract: Microsporidia are an abundant group of obligate intracellular parasites of other eukaryotes, including immunocompromised humans, but the molecular basis of their intracellular lifestyle and pathobiology are poorly understood. New genomes from a ... ...

Abstract	Microsporidia are an abundant group of obligate intracellular parasites of other eukaryotes, including immunocompromised humans, but the molecular basis of their intracellular lifestyle and pathobiology are poorly understood. New genomes from a taxonomically broad range of microsporidians, complemented by published expression data, provide an opportunity for comparative analyses to identify conserved and lineage-specific patterns of microsporidian genome evolution that have underpinned this success. In this study, we infer that a dramatic bottleneck in the last common microsporidian ancestor (LCMA) left a small conserved core of genes that was subsequently embellished by gene family expansion driven by gene acquisition in different lineages. Novel expressed protein families represent a substantial fraction of sequenced microsporidian genomes and are significantly enriched for signals consistent with secretion or membrane location. Further evidence of selection is inferred from the gain and reciprocal loss of functional domains between paralogous genes, for example, affecting transport proteins. Gene expansions among transporter families preferentially affect those that are located on the plasma membrane of model organisms, consistent with recruitment to plug conserved gaps in microsporidian biosynthesis and metabolism. Core microsporidian genes shared with other eukaryotes are enriched in orthologs that, in yeast, are highly expressed, highly connected, and often essential, consistent with strong negative selection against further reduction of the conserved gene set since the LCMA. Our study reveals that microsporidian genome evolution is a highly dynamic process that has balanced constraint, reductive evolution, and genome expansion during adaptation to an extraordinarily successful obligate intracellular lifestyle.
Keywords	Microsporidia ; biosynthesis ; eukaryotic cells ; evolution ; genes ; genomics ; parasites ; plasma membrane ; secretion ; transport proteins ; yeasts
Language	English
Size	p. 2285-2303.
Publishing place	Oxford University Press
Document type	Article
DOI	10.1093/gbe/evt184
Database	NAL-Catalogue (AGRICOLA)

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