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

Abstract

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.

Blowing Hot and Cold: Body Temperature and the Microbiome

“…Loss of diversity persists months after the heat stress itself ( 43 ) and is associated with decreased digestive efficiency ( 44 ). Furthermore, the bacterial symbionts of several insects collapse entirely under heat stress, with severe consequences for host vitality ( 21 – 23 , 45 ). Importantly, a heat shock gene variant in Buchnera , an obligate intracellular aphid symbiont, mediated the temperature sensitivity of the entire organism, including decreased fertility of the aphid during heat stress ( 23 ).…”

Diversity, Composition, and Specificity of the Philaenus spumarius Bacteriome

“…Indeed, the identified bacteria belonged to genera that have been recognized to manipulate insect reproduction via male-killing and parthenogenesis ( Rickettsia and Flavobacterium ) [ 59 , 60 ], supply amino acids and vitamins to their hosts ( Enterobacter , Sodalis , Rhodococcus , and Pantoea ) [ 61 , 62 , 63 , 64 ], or provide insecticide resistance to their host ( Rickettsia and Citrobacter ) [ 65 , 66 ]. Some are also capable of fixing nitrogen within the insect host ( Enterobacter ) [ 37 ], producing antibiotics ( Streptomyces ) [ 67 ], and providing insect protection against parasitoids (e.g., Serratia and Providencia ) [ 68 , 69 ] or heat stress ( Serratia and Sodalis ) [ 70 , 71 ]. The Halomonas genus was also detected in our study, but although members have been recognized as insect symbionts [ 50 ], their specific role has yet to be determined.…”

No evidence for direct thermal carryover effects on starvation tolerance in the obligate blood‐feeder, Glossina morsitans morsitans

“…Studies have shown that heat tolerance, longevity and/or fecundity are reduced when these bacterial symbionts are pharmaceutically eliminated (Dale & Welburn, 2001 ; Pais et al., 2008 ). Moreover, Sodalis glossinidius does not grow at temperatures above 31°C and is unable to survive for more than 48 h at 30°C (Roma et al., 2019 ). These bacteria were likely killed in the 31°C treatments and may have influenced the ability of tsetse to respond adaptively.…”