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

2019 ◽  
Vol 13 (11) ◽  
pp. e0007464 ◽  
Author(s):  
Jose Santinni Roma ◽  
Shaina D’Souza ◽  
Patrick J. Somers ◽  
Leah F. Cabo ◽  
Ruhan Farsin ◽  
...  
2019 ◽  
Author(s):  
Jose Santinni Roma ◽  
Shaina D’Souza ◽  
Patrick J. Somers ◽  
Leah F. Cabo ◽  
Ruhan Farsin ◽  
...  

ABSTRACTTsetse 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 25°C, and did not grow at temperatures above 30°C. 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 30°C, 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 30°C, while a higher temperature (37°C) 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 flies. 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.AUTHOR SUMMARYMicroorganisms associated with insects must cope with fluctuating temperatures. Because symbiotic bacteria influence the biology of their host, how they respond to temperature changes will have an impact on the host and other microorganisms in the host. The tsetse fly and its symbionts represent an important model system for studying thermal tolerance because the fly feeds exclusively on vertebrate blood and is thus exposed to dramatic temperature shifts. Tsetse flies house a microbial community that can consist of symbiotic and environmentally acquired bacteria, viruses, and parasitic African trypanosomes. This work, which makes use of tsetse’s commensal symbiont, Sodalis glossinidius, is significance because it represents the only examination of thermal tolerance mechanisms in a bacterium that resides indigenously within an arthropod disease vector. A better understanding of the biology of thermal tolerance in Sodalis provides insight into thermal stress survival in other insect symbionts and may yield information to help control vector-borne disease.


2010 ◽  
Vol 76 (11) ◽  
pp. 3486-3494 ◽  
Author(s):  
Nahomi Kaiwa ◽  
Takahiro Hosokawa ◽  
Yoshitomo Kikuchi ◽  
Naruo Nikoh ◽  
Xian Ying Meng ◽  
...  

ABSTRACT Symbiotic associations with midgut bacteria have been commonly found in diverse phytophagous heteropteran groups, where microbiological characterization of the symbiotic bacteria has been restricted to the stinkbug families Acanthosomatidae, Plataspidae, Pentatomidae, Alydidae, and Pyrrhocoridae. Here we investigated the midgut bacterial symbiont of Cantao ocellatus, a stinkbug of the family Scutelleridae. A specific gammaproteobacterium was consistently identified from the insects of different geographic origins. The bacterium was detected in all 116 insects collected from 9 natural host populations. Phylogenetic analyses revealed that the bacterium constitutes a distinct lineage in the Gammaproteobacteria, not closely related to gut symbionts of other stinkbugs. Diagnostic PCR and in situ hybridization demonstrated that the bacterium is extracellularly located in the midgut 4th section with crypts. Electron microscopy of the crypts revealed a peculiar histological configuration at the host-symbiont interface. Egg sterilization experiments confirmed that the bacterium is vertically transmitted to stinkbug nymphs via egg surface contamination. In addition to the gut symbiont, some individuals of C. ocellatus harbored another bacterial symbiont in their gonads, which was closely related to Sodalis glossinidius, the secondary endosymbiont of tsetse flies. Biological aspects of the primary gut symbiont and the secondary Sodalis-allied symbiont are discussed.


2003 ◽  
Vol 86 (1-2) ◽  
pp. 139-156 ◽  
Author(s):  
Robin J. Rowbury

Biological thermometers are cellular components or structures which sense increasing temperatures, interaction of the thermometer and the thermal stress bringing about the switching-on of inducible responses, with gradually enhanced levels of response induction following gradually increasing temperatures. In enterobacteria, for studies of such thermometers, generally induction of heat shock protein (HSP) synthesis has been examined, with experimental studies aiming to establish (often indirectly) how the temperature changes which initiate HSP synthesis are sensed; numerous other processes and responses show graded induction as temperature is increased, and how the temperature changes which induce these are sensed is also of interest. Several classes of intracellular component and structure have been proposed as enterobacterial thermometers, with the ribosome and the DnaK chaperone being the most favoured, although for many of the proposed intracellular thermometers, most of the evidence for their functioning in this way is indirect. In contrast to the above, the studies reviewed here firmly establish that for four distinct stress responses, which are switched-on gradually as temperature increases, temperature changes are sensed by extracellular components (extracellular sensing components, ESCs) i.e. there is firm and direct evidence for the occurrence of extracellular thermometers. All four thermometers described here are proteins, which appear to be distinct and different from each other, and on sensing thermal stress are activated by it to four distinct extracellular induction components (EICs), which interact with receptors on the surface of organisms to induce the appropriate responses. It is predicted that many other temperature-induced processes, including the synthesis of HSPs, will be switched-on following the activation of similar extracellular thermometers by thermal stimuli.


2018 ◽  
Vol 18 (S1) ◽  
Author(s):  
Güler Demirbas-Uzel ◽  
Linda De Vooght ◽  
Andrew G. Parker ◽  
Marc J. B. Vreysen ◽  
Robert L. Mach ◽  
...  

2010 ◽  
Vol 76 (13) ◽  
pp. 4130-4135 ◽  
Author(s):  
Takahiro Hosokawa ◽  
Yoshitomo Kikuchi ◽  
Naruo Nikoh ◽  
Xian-Ying Meng ◽  
Mantaro Hironaka ◽  
...  

ABSTRACT The stinkbug Parastrachia japonensis (Hemiptera: Parastrachiidae) is known for its prolonged prereproductive nonfeeding period, maternal care of eggs in an underground nest, and maternal collection and provisioning of food (fruits) for nymphs. A previous study suggested that a bacterial symbiont is involved in uric acid recycling in this insect during the nonfeeding period, but the identity of this symbiont has not been determined. Here we characterized a novel bacterial symbiont obtained from P. japonensis. Molecular phylogenetic analyses based on 16S rRNA, gyrB, and groEL gene sequences consistently indicated that this symbiont constituted a distinct lineage in the Gammaproteobacteria that has no close relatives but is allied with gut symbionts of acanthosomatid and plataspid stinkbugs, as well as with endocellular symbionts of sharpshooters, tsetse flies, and aphids. The symbiont genes had a remarkably AT-biased nucleotide composition and exhibited significantly accelerated molecular evolution. The symbiont genome was extremely reduced; its size was estimated to be 0.85 Mb. These results suggest that there has been an intimate host-symbiont association over evolutionary time. The symbiont was localized in swollen crypts in a posterior part of the midgut, which was a specialized symbiotic organ. The possibility that the symbiont is involved in uric acid recycling is discussed. The designation “Candidatus Benitsuchiphilus tojoi” is proposed for the symbiont.


2012 ◽  
Vol 2012 ◽  
pp. 1-11 ◽  
Author(s):  
Satish C. Boregowda ◽  
Robert E. Choate ◽  
Rodney Handy

The present study involves application of an open system entropy generation formulation to analyze human thermal stress responses. The time-series human thermal stress response data are obtained by conducting a simulation using a validated finite-element human thermal model (FEHTM). These simulated human thermal response data are used as an input to the entropy generation expression to obtain human entropy generation (HEG) values. The effects of variables such as air temperature, relative humidity, physical activity, and clothing on entropy generation are examined. A design of experiment (DOE) approach is utilized to study the interaction effects of air temperature and relative humidity on entropy generation. The study establishes the importance and utility of entropy generation as a holistic measure of human thermal physiological reaction to external and internal changes. This novel study has great potential for use in military medicine, rehabilitation, sports, and related applications.


2017 ◽  
Author(s):  
Joshua Louis Bonesso ◽  
William Leggat ◽  
Tracy Danielle Ainsworth

Elevated sea surface temperatures (SSTs) are linked to an increase in the frequency and severity of bleaching events due to temperatures exceeding corals’ upper thermal limits. The temperatures at which a breakdown of the coral-Symbiodinium endosymbiosis (coral bleaching) occurs are referred to as the upper thermal limits for the coral species. This breakdown of the endosymbiosis results in a reduction of corals’ nutritional uptake, growth, and tissue integrity. Periods of elevated sea surface temperature, thermal stress and coral bleaching are also linked to increased disease susceptibility and an increased frequency of storms which cause injury and physical damage to corals. Herein we aimed to determine the capacity of corals to regenerate and recover from injuries (removal of apical tips) sustained during periods of elevated sea surface temperatures which result in coral stress responses, but which do not result in coral bleaching (i.e. sub-bleaching thermal stress events). In this study, exposure of the species Acropora aspera to an elevated SST of 32°C (2°C below the bleaching threshold, 34°C) was found to result in reduced fluorescence of green fluorescent protein (GFP), reduced skeletal calcification and a lack of branch regrowth at the site of injury, compared to corals maintained under ambient SST conditions (26°C). Corals maintained under normal, ambient, sea surface temperatures expressed high GFP fluorescence at the injury site, underwent a rapid regeneration of the coral branch apical tip within 12 days of sustaining injury, and showed extensive regrowth of the coral skeleton. Taken together, our results have demonstrated that periods of sustained increased sea surface temperatures, below the corals’ bleaching threshold but above long-term summertime averages, impair coral recovery from damage, regardless of the onset or occurrence of coral bleaching .


2021 ◽  
Author(s):  
◽  
Anne Wietheger

<p>Coral bleaching, the loss of symbiotic dinoflagellate algae (genus Symbiodinium) and/or photosynthetic algal pigments from their coral host has become a regular occurrence in the last few decades due to increasing seawater temperatures. A key consideration in bleaching susceptibility is the symbiotic alga‘s physiology and its capacity to deal with abiotic stress; oxidative stress is of particular interest given that this can arise from thermally induced photosynthetic dysfunction. The aim of this study was to compare the effects of thermal and oxidative stress on the photosynthetic performance of a range of Symbiodinium clades and types (i.e. sub-clades) in different states of symbiosis (in hospite, freshly isolated and in culture). Whether the responses to these two stressors are related was investigated; in particular, it was hypothesised that more thermally sensitive types would be more sensitive to oxidative stress. Furthermore, the study aimed to elucidate the role of antioxidants in the observed stress responses. The specific objectives were 1) to establish whether different types of cultured Symbiodinium have dissimilar sensitivities to oxidative stress, induced by hydrogen peroxide (H₂O₂), and whether these are related to their thermal sensitivities; 2) measure the activity and relative amounts of specific reactive oxygen species (ROS) in different types of cultured Symbiodinium in response to thermal and oxidative stress induced by H₂O₂; 3) measure total antioxidant activity in different cultured Symbiodinium types when under oxidative stress; and 4) compare and contrast the responses of different Symbiodinium types to thermal and oxidative stress when in hospite (i.e. in corals) and freshly isolated. In this study, I showed that different Symbiodinium clades and types can differ widely in their responses to both thermal and oxidative stress. This was indicated by photosynthetic performance measured by chlorophyll fluorescence, and differences in the quantity of specific ROS measured via fluorescent probes and flow cytometry. For instance, when adding H₂O₂ to Symbiodinium F1, originally from Hawaii, a decrease of > 99% in maximum quantum yield (Fv/Fm) was displayed, while there was no change in Fv/Fm in the temperate Symbiodinium A1, freshly isolated from the anemone Anthopleura aureoradiata from New Zealand. When comparing the difference in ROS production between the control (26 °C) and a thermal stress treatment (35 °C), type E1 from Okinawa showed no difference in any of the measured ROS. In contrast, a different A1 type from the Gulf of Aqaba displayed an increase in the overall production of ROS, and more specifically in the production of superoxide. Symbiodinium types also displayed differential oxidative stress resistance, which was apparent from their antioxidant activities; in particular, total antioxidant capacity was measured by the ferric reducing antioxidant potential (FRAP) and cellular antioxidant activity (CAA) assays. For example, the aforementioned Symbiodinium types, A1 from the Gulf of Aqaba and F1, increased their antioxidant activities with increasing H₂O₂ concentrations. Meanwhile, type E1 displayed higher baseline levels of antioxidants in comparison to the other two types (A1, F1), which then decreased with increasing H₂O₂. Specific activities of superoxide dismutase and ascorbate peroxidase were also measured. Stress susceptibility appears to be related both to Symbiodinium type and geographic origin, but greater sensitivity to thermal stress did not necessarily correlate with greater susceptibility to oxidative stress. The exact relationship between thermal and oxidative sensitivities in Symbiodinium spp. remains elusive, but it is suggested that different types might follow different strategies for dealing with stress. I propose that some Symbiodinium types rely more on photo-protection when exposed to thermal stress (and hence cope less with oxidative stress), while other types depend more on antioxidants and oxidative stress resistance. The latter might be the better strategy for types from more variable environments, such as higher latitude reefs or intertidal regions, where potentially stressful conditions may be encountered more frequently. This study gives new insights into the variability of stress responses in the genus Symbiodinium, and the complex relationship between thermal and oxidative stress. The implications of these findings for coral bleaching susceptibility and the biogeographic distribution of different Symbiodinium types are discussed.</p>


2021 ◽  
Vol 15 (1) ◽  
pp. e0008267
Author(s):  
Edward Edmond Makhulu ◽  
Jandouwe Villinger ◽  
Vincent Owino Adunga ◽  
Maamun M. Jeneby ◽  
Edwin Murungi Kimathi ◽  
...  

African trypanosomiasis (AT) is a neglected disease of both humans and animals caused by Trypanosoma parasites, which are transmitted by obligate hematophagous tsetse flies (Glossina spp.). Knowledge on tsetse fly vertebrate hosts and the influence of tsetse endosymbionts on trypanosome presence, especially in wildlife-human-livestock interfaces, is limited. We identified tsetse species, their blood-meal sources, and correlations between endosymbionts and trypanosome presence in tsetse flies from the trypanosome-endemic Maasai Mara National Reserve (MMNR) in Kenya. Among 1167 tsetse flies (1136 Glossina pallidipes, 31 Glossina swynnertoni) collected from 10 sampling sites, 28 (2.4%) were positive by PCR for trypanosome DNA, most (17/28) being of Trypanosoma vivax species. Blood-meal analyses based on high-resolution melting analysis of vertebrate cytochrome c oxidase 1 and cytochrome b gene PCR products (n = 354) identified humans as the most common vertebrate host (37%), followed by hippopotamus (29.1%), African buffalo (26.3%), elephant (3.39%), and giraffe (0.84%). Flies positive for trypanosome DNA had fed on hippopotamus and buffalo. Tsetse flies were more likely to be positive for trypanosomes if they had the Sodalis glossinidius endosymbiont (P = 0.0002). These findings point to complex interactions of tsetse flies with trypanosomes, endosymbionts, and diverse vertebrate hosts in wildlife ecosystems such as in the MMNR, which should be considered in control programs. These interactions may contribute to the maintenance of tsetse populations and/or persistent circulation of African trypanosomes. Although the African buffalo is a key reservoir of AT, the higher proportion of hippopotamus blood-meals in flies with trypanosome DNA indicates that other wildlife species may be important in AT transmission. No trypanosomes associated with human disease were identified, but the high proportion of human blood-meals identified are indicative of human African trypanosomiasis risk. Our results add to existing data suggesting that Sodalis endosymbionts are associated with increased trypanosome presence in tsetse flies.


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