Insight into the Transmission Biology and Species-Specific Functional Capabilities of Tsetse (Diptera: Glossinidae) Obligate Symbiont <italic toggle="yes">Wigglesworthia</italic>

ABSTRACT Ancient endosymbionts have been associated with extreme genome structural stability with little differentiation in gene inventory between sister species. Tsetse flies (Diptera: Glossinidae) harbor an obligate endosymbiont, Wigglesworthia, which has coevolved with the Glossina radiation. We...

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Autores principales: Rita V. M. Rio, Rebecca E. Symula, Jingwen Wang, Claudia Lohs, Yi-neng Wu, Anna K. Snyder, Robert D. Bjornson, Kenshiro Oshima, Bryan S. Biehl, Nicole T. Perna, Masahira Hattori, Serap Aksoy
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Publicado: American Society for Microbiology 2012
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spelling oai:doaj.org-article:998394c6dbe941ea8efe35ae96504c882021-11-15T15:39:02ZInsight into the Transmission Biology and Species-Specific Functional Capabilities of Tsetse (Diptera: Glossinidae) Obligate Symbiont <italic toggle="yes">Wigglesworthia</italic>10.1128/mBio.00240-112150-7511https://doaj.org/article/998394c6dbe941ea8efe35ae96504c882012-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00240-11https://doaj.org/toc/2150-7511ABSTRACT Ancient endosymbionts have been associated with extreme genome structural stability with little differentiation in gene inventory between sister species. Tsetse flies (Diptera: Glossinidae) harbor an obligate endosymbiont, Wigglesworthia, which has coevolved with the Glossina radiation. We report on the ~720-kb Wigglesworthia genome and its associated plasmid from Glossina morsitans morsitans and compare them to those of the symbiont from Glossina brevipalpis. While there was overall high synteny between the two genomes, a large inversion was noted. Furthermore, symbiont transcriptional analyses demonstrated host tissue and development-specific gene expression supporting robust transcriptional regulation in Wigglesworthia, an unprecedented observation in other obligate mutualist endosymbionts. Expression and immunohistochemistry confirmed the role of flagella during the vertical transmission process from mother to intrauterine progeny. The expression of nutrient provisioning genes (thiC and hemH) suggests that Wigglesworthia may function in dietary supplementation tailored toward host development. Furthermore, despite extensive conservation, unique genes were identified within both symbiont genomes that may result in distinct metabolomes impacting host physiology. One of these differences involves the chorismate, phenylalanine, and folate biosynthetic pathways, which are uniquely present in Wigglesworthia morsitans. Interestingly, African trypanosomes are auxotrophs for phenylalanine and folate and salvage both exogenously. It is possible that W. morsitans contributes to the higher parasite susceptibility of its host species. IMPORTANCE Genomic stasis has historically been associated with obligate endosymbionts and their sister species. Here we characterize the Wigglesworthia genome of the tsetse fly species Glossina morsitans and compare it to its sister genome within G. brevipalpis. The similarity and variation between the genomes enabled specific hypotheses regarding functional biology. Expression analyses indicate significant levels of transcriptional regulation and support development- and tissue-specific functional roles for the symbiosis previously not observed in obligate mutualist symbionts. Retention of the genetically expensive flagella within these small genomes was demonstrated to be significant in symbiont transmission and tailored to the unique tsetse fly reproductive biology. Distinctions in metabolomes were also observed. We speculate an additional role for Wigglesworthia symbiosis where infections with pathogenic trypanosomes may depend upon symbiont species-specific metabolic products and thus influence the vector competence traits of different tsetse fly host species.Rita V. M. RioRebecca E. SymulaJingwen WangClaudia LohsYi-neng WuAnna K. SnyderRobert D. BjornsonKenshiro OshimaBryan S. BiehlNicole T. PernaMasahira HattoriSerap AksoyAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 3, Iss 1 (2012)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Rita V. M. Rio
Rebecca E. Symula
Jingwen Wang
Claudia Lohs
Yi-neng Wu
Anna K. Snyder
Robert D. Bjornson
Kenshiro Oshima
Bryan S. Biehl
Nicole T. Perna
Masahira Hattori
Serap Aksoy
Insight into the Transmission Biology and Species-Specific Functional Capabilities of Tsetse (Diptera: Glossinidae) Obligate Symbiont <italic toggle="yes">Wigglesworthia</italic>
description ABSTRACT Ancient endosymbionts have been associated with extreme genome structural stability with little differentiation in gene inventory between sister species. Tsetse flies (Diptera: Glossinidae) harbor an obligate endosymbiont, Wigglesworthia, which has coevolved with the Glossina radiation. We report on the ~720-kb Wigglesworthia genome and its associated plasmid from Glossina morsitans morsitans and compare them to those of the symbiont from Glossina brevipalpis. While there was overall high synteny between the two genomes, a large inversion was noted. Furthermore, symbiont transcriptional analyses demonstrated host tissue and development-specific gene expression supporting robust transcriptional regulation in Wigglesworthia, an unprecedented observation in other obligate mutualist endosymbionts. Expression and immunohistochemistry confirmed the role of flagella during the vertical transmission process from mother to intrauterine progeny. The expression of nutrient provisioning genes (thiC and hemH) suggests that Wigglesworthia may function in dietary supplementation tailored toward host development. Furthermore, despite extensive conservation, unique genes were identified within both symbiont genomes that may result in distinct metabolomes impacting host physiology. One of these differences involves the chorismate, phenylalanine, and folate biosynthetic pathways, which are uniquely present in Wigglesworthia morsitans. Interestingly, African trypanosomes are auxotrophs for phenylalanine and folate and salvage both exogenously. It is possible that W. morsitans contributes to the higher parasite susceptibility of its host species. IMPORTANCE Genomic stasis has historically been associated with obligate endosymbionts and their sister species. Here we characterize the Wigglesworthia genome of the tsetse fly species Glossina morsitans and compare it to its sister genome within G. brevipalpis. The similarity and variation between the genomes enabled specific hypotheses regarding functional biology. Expression analyses indicate significant levels of transcriptional regulation and support development- and tissue-specific functional roles for the symbiosis previously not observed in obligate mutualist symbionts. Retention of the genetically expensive flagella within these small genomes was demonstrated to be significant in symbiont transmission and tailored to the unique tsetse fly reproductive biology. Distinctions in metabolomes were also observed. We speculate an additional role for Wigglesworthia symbiosis where infections with pathogenic trypanosomes may depend upon symbiont species-specific metabolic products and thus influence the vector competence traits of different tsetse fly host species.
format article
author Rita V. M. Rio
Rebecca E. Symula
Jingwen Wang
Claudia Lohs
Yi-neng Wu
Anna K. Snyder
Robert D. Bjornson
Kenshiro Oshima
Bryan S. Biehl
Nicole T. Perna
Masahira Hattori
Serap Aksoy
author_facet Rita V. M. Rio
Rebecca E. Symula
Jingwen Wang
Claudia Lohs
Yi-neng Wu
Anna K. Snyder
Robert D. Bjornson
Kenshiro Oshima
Bryan S. Biehl
Nicole T. Perna
Masahira Hattori
Serap Aksoy
author_sort Rita V. M. Rio
title Insight into the Transmission Biology and Species-Specific Functional Capabilities of Tsetse (Diptera: Glossinidae) Obligate Symbiont <italic toggle="yes">Wigglesworthia</italic>
title_short Insight into the Transmission Biology and Species-Specific Functional Capabilities of Tsetse (Diptera: Glossinidae) Obligate Symbiont <italic toggle="yes">Wigglesworthia</italic>
title_full Insight into the Transmission Biology and Species-Specific Functional Capabilities of Tsetse (Diptera: Glossinidae) Obligate Symbiont <italic toggle="yes">Wigglesworthia</italic>
title_fullStr Insight into the Transmission Biology and Species-Specific Functional Capabilities of Tsetse (Diptera: Glossinidae) Obligate Symbiont <italic toggle="yes">Wigglesworthia</italic>
title_full_unstemmed Insight into the Transmission Biology and Species-Specific Functional Capabilities of Tsetse (Diptera: Glossinidae) Obligate Symbiont <italic toggle="yes">Wigglesworthia</italic>
title_sort insight into the transmission biology and species-specific functional capabilities of tsetse (diptera: glossinidae) obligate symbiont <italic toggle="yes">wigglesworthia</italic>
publisher American Society for Microbiology
publishDate 2012
url https://doaj.org/article/998394c6dbe941ea8efe35ae96504c88
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