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...
Main Authors: | , , , , , , , |
---|---|
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 |
id |
doaj-8aeed0f3496c4aa3bbd6f40ba0fd525c |
---|---|
record_format |
Article |
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 |
work_keys_str_mv |
AT josesantinniroma thermalstressresponsesofsodalisglossinidiusanindigenousbacterialsymbiontofhematophagoustsetseflies AT shainadsouza thermalstressresponsesofsodalisglossinidiusanindigenousbacterialsymbiontofhematophagoustsetseflies AT patrickjsomers thermalstressresponsesofsodalisglossinidiusanindigenousbacterialsymbiontofhematophagoustsetseflies AT leahfcabo thermalstressresponsesofsodalisglossinidiusanindigenousbacterialsymbiontofhematophagoustsetseflies AT ruhanfarsin thermalstressresponsesofsodalisglossinidiusanindigenousbacterialsymbiontofhematophagoustsetseflies AT serapaksoy thermalstressresponsesofsodalisglossinidiusanindigenousbacterialsymbiontofhematophagoustsetseflies AT laurajrunyenjanecky thermalstressresponsesofsodalisglossinidiusanindigenousbacterialsymbiontofhematophagoustsetseflies AT brianlweiss thermalstressresponsesofsodalisglossinidiusanindigenousbacterialsymbiontofhematophagoustsetseflies |
_version_ |
1721391044237459456 |