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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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
Language:English
Published: Public Library of Science (PLoS) 2019-11-01
Series:PLoS Neglected Tropical Diseases
Online Access:https://doi.org/10.1371/journal.pntd.0007464
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spelling doaj-8aeed0f3496c4aa3bbd6f40ba0fd525c2021-06-08T04:31:35ZengPublic Library of Science (PLoS)PLoS Neglected Tropical Diseases1935-27271935-27352019-11-011311e000746410.1371/journal.pntd.0007464Thermal stress responses of Sodalis glossinidius, an indigenous bacterial symbiont of hematophagous tsetse flies.Jose Santinni RomaShaina D'SouzaPatrick J SomersLeah F CaboRuhan FarsinSerap AksoyLaura J Runyen-JaneckyBrian L WeissTsetse 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.https://doi.org/10.1371/journal.pntd.0007464
collection DOAJ
language English
format Article
sources DOAJ
author Jose Santinni Roma
Shaina D'Souza
Patrick J Somers
Leah F Cabo
Ruhan Farsin
Serap Aksoy
Laura J Runyen-Janecky
Brian L Weiss
spellingShingle 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.
PLoS Neglected Tropical Diseases
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)
series PLoS Neglected Tropical Diseases
issn 1935-2727
1935-2735
publishDate 2019-11-01
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.
url https://doi.org/10.1371/journal.pntd.0007464
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