Thermal stress responses of Sodalis glossinidius, an indigenous bacterial symbiont of hematophagous tsetse flies.

Tsetse flies (Diptera: Glossinidae) house a taxonomically diverse microbiota that includes environmentally acquired bacteria, maternally transmitted symbiotic bacteria, and pathogenic African trypanosomes. Sodalis glossinidius, which is a facultative symbiont that resides intra and extracellularly w...

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Published in:PLOS Neglected Tropical Diseases
Main Authors: Jose Santinni Roma, Shaina D'Souza, Patrick J Somers, Leah F Cabo, Ruhan Farsin, Serap Aksoy, Laura J Runyen-Janecky, Brian L Weiss
Format: Article in Journal/Newspaper
Language:English
Published: Public Library of Science (PLoS) 2019
Subjects:
Online Access:https://doi.org/10.1371/journal.pntd.0007464
https://doaj.org/article/8aeed0f3496c4aa3bbd6f40ba0fd525c
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spelling ftdoajarticles:oai:doaj.org/article:8aeed0f3496c4aa3bbd6f40ba0fd525c 2023-05-15T15:16:41+02:00 Thermal stress responses of Sodalis glossinidius, an indigenous bacterial symbiont of hematophagous tsetse flies. Jose Santinni Roma Shaina D'Souza Patrick J Somers Leah F Cabo Ruhan Farsin Serap Aksoy Laura J Runyen-Janecky Brian L Weiss 2019-11-01T00:00:00Z https://doi.org/10.1371/journal.pntd.0007464 https://doaj.org/article/8aeed0f3496c4aa3bbd6f40ba0fd525c EN eng Public Library of Science (PLoS) https://doi.org/10.1371/journal.pntd.0007464 https://doaj.org/toc/1935-2727 https://doaj.org/toc/1935-2735 1935-2727 1935-2735 doi:10.1371/journal.pntd.0007464 https://doaj.org/article/8aeed0f3496c4aa3bbd6f40ba0fd525c PLoS Neglected Tropical Diseases, Vol 13, Iss 11, p e0007464 (2019) Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 article 2019 ftdoajarticles https://doi.org/10.1371/journal.pntd.0007464 2022-12-31T13:53:10Z Tsetse flies (Diptera: Glossinidae) house a taxonomically diverse microbiota that includes environmentally acquired bacteria, maternally transmitted symbiotic bacteria, and pathogenic African trypanosomes. Sodalis glossinidius, which is a facultative symbiont that resides intra and extracellularly within multiple tsetse tissues, has been implicated as a mediator of trypanosome infection establishment in the fly's gut. Tsetse's gut-associated population of Sodalis are subjected to marked temperature fluctuations each time their ectothermic fly host imbibes vertebrate blood. The molecular mechanisms that Sodalis employs to deal with this heat stress are unknown. In this study, we examined the thermal tolerance and heat shock response of Sodalis. When grown on BHI agar plates, the bacterium exhibited the most prolific growth at 25oC, and did not grow at temperatures above 30oC. Growth on BHI agar plates at 31°C was dependent on either the addition of blood to the agar or reduction in oxygen levels. Sodalis was viable in liquid cultures for 24 hours at 30oC, but began to die upon further exposure. The rate of death increased with increased temperature. Similarly, Sodalis was able to survive for 48 hours within tsetse flies housed at 30oC, while a higher temperature (37oC) was lethal. Sodalis' genome contains homologues of the heat shock chaperone protein-encoding genes dnaK, dnaJ, and grpE, and their expression was up-regulated in thermally stressed Sodalis, both in vitro and in vivo within tsetse fly midguts. Arrested growth of E. coli dnaK, dnaJ, or grpE mutants under thermal stress was reversed when the cells were transformed with a low copy plasmid that encoded the Sodalis homologues of these genes. The information contained in this study provides insight into how arthropod vector enteric commensals, many of which mediate their host's ability to transmit pathogens, mitigate heat shock associated with the ingestion of a blood meal. Article in Journal/Newspaper Arctic Directory of Open Access Journals: DOAJ Articles Arctic PLOS Neglected Tropical Diseases 13 11 e0007464
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
spellingShingle Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
Jose Santinni Roma
Shaina D'Souza
Patrick J Somers
Leah F Cabo
Ruhan Farsin
Serap Aksoy
Laura J Runyen-Janecky
Brian L Weiss
Thermal stress responses of Sodalis glossinidius, an indigenous bacterial symbiont of hematophagous tsetse flies.
topic_facet Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
description Tsetse flies (Diptera: Glossinidae) house a taxonomically diverse microbiota that includes environmentally acquired bacteria, maternally transmitted symbiotic bacteria, and pathogenic African trypanosomes. Sodalis glossinidius, which is a facultative symbiont that resides intra and extracellularly within multiple tsetse tissues, has been implicated as a mediator of trypanosome infection establishment in the fly's gut. Tsetse's gut-associated population of Sodalis are subjected to marked temperature fluctuations each time their ectothermic fly host imbibes vertebrate blood. The molecular mechanisms that Sodalis employs to deal with this heat stress are unknown. In this study, we examined the thermal tolerance and heat shock response of Sodalis. When grown on BHI agar plates, the bacterium exhibited the most prolific growth at 25oC, and did not grow at temperatures above 30oC. Growth on BHI agar plates at 31°C was dependent on either the addition of blood to the agar or reduction in oxygen levels. Sodalis was viable in liquid cultures for 24 hours at 30oC, but began to die upon further exposure. The rate of death increased with increased temperature. Similarly, Sodalis was able to survive for 48 hours within tsetse flies housed at 30oC, while a higher temperature (37oC) was lethal. Sodalis' genome contains homologues of the heat shock chaperone protein-encoding genes dnaK, dnaJ, and grpE, and their expression was up-regulated in thermally stressed Sodalis, both in vitro and in vivo within tsetse fly midguts. Arrested growth of E. coli dnaK, dnaJ, or grpE mutants under thermal stress was reversed when the cells were transformed with a low copy plasmid that encoded the Sodalis homologues of these genes. The information contained in this study provides insight into how arthropod vector enteric commensals, many of which mediate their host's ability to transmit pathogens, mitigate heat shock associated with the ingestion of a blood meal.
format Article in Journal/Newspaper
author Jose Santinni Roma
Shaina D'Souza
Patrick J Somers
Leah F Cabo
Ruhan Farsin
Serap Aksoy
Laura J Runyen-Janecky
Brian L Weiss
author_facet Jose Santinni Roma
Shaina D'Souza
Patrick J Somers
Leah F Cabo
Ruhan Farsin
Serap Aksoy
Laura J Runyen-Janecky
Brian L Weiss
author_sort Jose Santinni Roma
title Thermal stress responses of Sodalis glossinidius, an indigenous bacterial symbiont of hematophagous tsetse flies.
title_short Thermal stress responses of Sodalis glossinidius, an indigenous bacterial symbiont of hematophagous tsetse flies.
title_full Thermal stress responses of Sodalis glossinidius, an indigenous bacterial symbiont of hematophagous tsetse flies.
title_fullStr Thermal stress responses of Sodalis glossinidius, an indigenous bacterial symbiont of hematophagous tsetse flies.
title_full_unstemmed Thermal stress responses of Sodalis glossinidius, an indigenous bacterial symbiont of hematophagous tsetse flies.
title_sort thermal stress responses of sodalis glossinidius, an indigenous bacterial symbiont of hematophagous tsetse flies.
publisher Public Library of Science (PLoS)
publishDate 2019
url https://doi.org/10.1371/journal.pntd.0007464
https://doaj.org/article/8aeed0f3496c4aa3bbd6f40ba0fd525c
geographic Arctic
geographic_facet Arctic
genre Arctic
genre_facet Arctic
op_source PLoS Neglected Tropical Diseases, Vol 13, Iss 11, p e0007464 (2019)
op_relation https://doi.org/10.1371/journal.pntd.0007464
https://doaj.org/toc/1935-2727
https://doaj.org/toc/1935-2735
1935-2727
1935-2735
doi:10.1371/journal.pntd.0007464
https://doaj.org/article/8aeed0f3496c4aa3bbd6f40ba0fd525c
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container_title PLOS Neglected Tropical Diseases
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