Infection Dynamics and Immune Response in a Newly Described <italic toggle="yes">Drosophila</italic>-Trypanosomatid Association

ABSTRACT Trypanosomatid parasites are significant causes of human disease and are ubiquitous in insects. Despite the importance of Drosophila melanogaster as a model of infection and immunity and a long awareness that trypanosomatid infection is common in the genus, no trypanosomatid parasites natur...

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Autores principales:	Phineas T. Hamilton, Jan Votýpka, Anna Dostálová, Vyacheslav Yurchenko, Nathan H. Bird, Julius Lukeš, Bruno Lemaitre, Steve J. Perlman
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a82d6a797dc54b29b7bbdffabb8637a4
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spelling	oai:doaj.org-article:a82d6a797dc54b29b7bbdffabb8637a42021-11-15T15:41:30ZInfection Dynamics and Immune Response in a Newly Described <italic toggle="yes">Drosophila</italic>-Trypanosomatid Association10.1128/mBio.01356-152150-7511https://doaj.org/article/a82d6a797dc54b29b7bbdffabb8637a42015-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01356-15https://doaj.org/toc/2150-7511ABSTRACT Trypanosomatid parasites are significant causes of human disease and are ubiquitous in insects. Despite the importance of Drosophila melanogaster as a model of infection and immunity and a long awareness that trypanosomatid infection is common in the genus, no trypanosomatid parasites naturally infecting Drosophila have been characterized. Here, we establish a new model of trypanosomatid infection in Drosophila—Jaenimonas drosophilae, gen. et sp. nov. As far as we are aware, this is the first Drosophila-parasitic trypanosomatid to be cultured and characterized. Through experimental infections, we find that Drosophila falleni, the natural host, is highly susceptible to infection, leading to a substantial decrease in host fecundity. J. drosophilae has a broad host range, readily infecting a number of Drosophila species, including D. melanogaster, with oral infection of D. melanogaster larvae resulting in the induction of numerous immune genes. When injected into adult hemolymph, J. drosophilae kills D. melanogaster, although interestingly, neither the Imd nor the Toll pathway is induced and Imd mutants do not show increased susceptibility to infection. In contrast, mutants deficient in drosocrystallin, a major component of the peritrophic matrix, are more severely infected during oral infection, suggesting that the peritrophic matrix plays an important role in mediating trypanosomatid infection in Drosophila. This work demonstrates that the J. drosophilae-Drosophila system can be a powerful model to uncover the effects of trypanosomatids in their insect hosts. IMPORTANCE Trypanosomatid parasites are ubiquitous in insects and are significant causes of disease when vectored to humans by blood-feeding insects. In recent decades, Drosophila has emerged as the predominant insect model of infection and immunity and is also known to be infected by trypanosomatids at high rates in the wild. Despite this, there has been almost no work on their trypanosomatid parasites, in part because Drosophila-specific trypanosomatids have been resistant to culturing. Here, we present the first isolation and detailed characterization of a trypanosomatid from Drosophila, finding that it represents a new genus and species, Jaenimonas drosophilae. Using this parasite, we conducted a series of experiments that revealed many of the unknown aspects of trypanosomatid infection in Drosophila, including host range, transmission biology, dynamics of infection, and host immune response. Taken together, this work establishes J. drosophilae as a powerful new opportunity to study trypanosomatid infections in insects.Phineas T. HamiltonJan VotýpkaAnna DostálováVyacheslav YurchenkoNathan H. BirdJulius LukešBruno LemaitreSteve J. PerlmanAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 5 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Phineas T. Hamilton Jan Votýpka Anna Dostálová Vyacheslav Yurchenko Nathan H. Bird Julius Lukeš Bruno Lemaitre Steve J. Perlman Infection Dynamics and Immune Response in a Newly Described <italic toggle="yes">Drosophila</italic>-Trypanosomatid Association
description	ABSTRACT Trypanosomatid parasites are significant causes of human disease and are ubiquitous in insects. Despite the importance of Drosophila melanogaster as a model of infection and immunity and a long awareness that trypanosomatid infection is common in the genus, no trypanosomatid parasites naturally infecting Drosophila have been characterized. Here, we establish a new model of trypanosomatid infection in Drosophila—Jaenimonas drosophilae, gen. et sp. nov. As far as we are aware, this is the first Drosophila-parasitic trypanosomatid to be cultured and characterized. Through experimental infections, we find that Drosophila falleni, the natural host, is highly susceptible to infection, leading to a substantial decrease in host fecundity. J. drosophilae has a broad host range, readily infecting a number of Drosophila species, including D. melanogaster, with oral infection of D. melanogaster larvae resulting in the induction of numerous immune genes. When injected into adult hemolymph, J. drosophilae kills D. melanogaster, although interestingly, neither the Imd nor the Toll pathway is induced and Imd mutants do not show increased susceptibility to infection. In contrast, mutants deficient in drosocrystallin, a major component of the peritrophic matrix, are more severely infected during oral infection, suggesting that the peritrophic matrix plays an important role in mediating trypanosomatid infection in Drosophila. This work demonstrates that the J. drosophilae-Drosophila system can be a powerful model to uncover the effects of trypanosomatids in their insect hosts. IMPORTANCE Trypanosomatid parasites are ubiquitous in insects and are significant causes of disease when vectored to humans by blood-feeding insects. In recent decades, Drosophila has emerged as the predominant insect model of infection and immunity and is also known to be infected by trypanosomatids at high rates in the wild. Despite this, there has been almost no work on their trypanosomatid parasites, in part because Drosophila-specific trypanosomatids have been resistant to culturing. Here, we present the first isolation and detailed characterization of a trypanosomatid from Drosophila, finding that it represents a new genus and species, Jaenimonas drosophilae. Using this parasite, we conducted a series of experiments that revealed many of the unknown aspects of trypanosomatid infection in Drosophila, including host range, transmission biology, dynamics of infection, and host immune response. Taken together, this work establishes J. drosophilae as a powerful new opportunity to study trypanosomatid infections in insects.
format	article
author	Phineas T. Hamilton Jan Votýpka Anna Dostálová Vyacheslav Yurchenko Nathan H. Bird Julius Lukeš Bruno Lemaitre Steve J. Perlman
author_facet	Phineas T. Hamilton Jan Votýpka Anna Dostálová Vyacheslav Yurchenko Nathan H. Bird Julius Lukeš Bruno Lemaitre Steve J. Perlman
author_sort	Phineas T. Hamilton
title	Infection Dynamics and Immune Response in a Newly Described <italic toggle="yes">Drosophila</italic>-Trypanosomatid Association
title_short	Infection Dynamics and Immune Response in a Newly Described <italic toggle="yes">Drosophila</italic>-Trypanosomatid Association
title_full	Infection Dynamics and Immune Response in a Newly Described <italic toggle="yes">Drosophila</italic>-Trypanosomatid Association
title_fullStr	Infection Dynamics and Immune Response in a Newly Described <italic toggle="yes">Drosophila</italic>-Trypanosomatid Association
title_full_unstemmed	Infection Dynamics and Immune Response in a Newly Described <italic toggle="yes">Drosophila</italic>-Trypanosomatid Association
title_sort	infection dynamics and immune response in a newly described <italic toggle="yes">drosophila</italic>-trypanosomatid association
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/a82d6a797dc54b29b7bbdffabb8637a4
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Infection Dynamics and Immune Response in a Newly Described <italic toggle="yes">Drosophila</italic>-Trypanosomatid Association

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