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Response to thermal and infection stresses in an American vector of visceral leishmaniasis

Kelsilandia A. Martins, Caroline S. Morais, Susan J. Broughton, Claudio R. Lazzari, Paul A. Bates, Marcos H. Pereira, Rod J. Dillon

Preprint posted on November 23, 2020 https://www.biorxiv.org/content/10.1101/2020.11.23.373100v1

Leishmania: What happens when an insect ingests a big warm blood meal?

Selected by Mariana De Niz

Categories: cell biology

Background

The phlebotomine sandfly Lutzomyia longipalpis is the primary insect vector of visceral leishmaniasis in the Americas. Parasite transmission happens when infected sandfly females take a bloodmeal from a human, and in doing so, inject the Leishmania metacyclic promastigote.  The ambient temperature is an abiotic factor that can influence insect fitness in terms of their development, reproduction and survival. Moreover, in hematophagous insects, additional changes can occur due to their feeding on the blood of homeothermic vertebrates. For instance, the body temperature of mammals can vary in a range of 30-38°C. Additionally, insect vectors have evolved to be able to ingest large amounts of blood in a short amount of time to avoid potentially fatal host recognition by the hosts. Thus, blood-feeding results in both, a dramatic increase in body size, and potentially an increase in temperature, in a relatively short amount of time. A rapid change in body temperature in insects can influence multiple processes including protein synthesis, metamorphosis, cell division, and hormone secretion. The authors propose that the impact of temperature has been ignored in previous investigations of stress-induced responses by the vector, such as during a bloodmeal or a Leishmania infection. Therefore, in their work, Martins et al (1) explored the interaction of Lu. Longipalpis with temperature, evaluating sandfly behaviour and heat shock protein expression across a thermal gradient following surgar or blood-feeding, and infection with Leishmania mexicana.

Key findings and developments

The authors divided their findings into thermo-preference, thermography and heat shock protein changes.

Relation between bloodmeal, thermopreference, infection status, age, oviposition and Leishmania mexicanadevelopment. Without a temperature gradient, insect distribution was independent of sex, however it suggests that females walk further and faster than males. Upon establishment of a temperature gradient, the distribution of males and females remained unchanged- with sandflies spending significant time in some specific zones of cold and warm extremes. A 3 day infection did not alter this behaviour in females, and altogether, females seemed to prefer one specific zone in the thermogradient. Blood fed and infected females at this time post-feed, seemed to prefer cold extreme than other sections of the thermal gradient. At 6 days post blood feed (infected or not), the behaviour of infected and non-infected flies remained indistinguishable in the various sections of the gradient, but it was no longer specific to the cold extreme (as at 3 days post-feed). Actually, these females also now spent more time in the hot extreme of the thermal gradient. Meanwhile, activity level, distance traveled and speed, remained unaltered across groups. The authors then evaluated if the age of the females (with or without a bloodmeal) impacted their thermal choice preferences, and found that this was not the case. However, upon looking at activity they found that infected females were slower and walked less on the third day post infected feed. Regardless of age or infection status, blood-fed sandflies spent more time, and visited more frequently, the coldest area of the thermogradient. The difference in temperature choices on the 3rd and 6th days post blood ingestion continued when oviposition was followed. Temperature was found to influence both oviposition and mortality proportions of Lu. longipalpis females. Females kept at 30°C had no remains of blood inside their gut, oocytes were in an advanced state of development, and all females were found dead, leaving eggs in 85% of pots. Conversely, females at the same time post-feed, kept at 20°C remained with a large amount of undigested blood inside their gut, oocytes were poorly developed, and eggs were only seen in pots at day 4 post-feed, but survival of the females was much higher by day 6 after oviposition, compared to groups kept at 24°C or 30°C. Moreover, temperature affected the development of L. mexicana, impacting the first day that flagellate forms were found within sandflies. The proportion of infected females 6 days post-infection was highest in sandflies kept at 20°C, and was 0% in sandflies kept at 30°C.

Thermography. The authors report that after some probing bites, Lu. longipalpis begin to ingest the bloodmeal and remain in the same place until the end of the feed. During this time, the body temperature of the insects increases homogeneously and then remains constant throughout ingestion at around 35°C, until the end of the feed, revealing a thermoregulatory behaviour.

Heat shock proteins. The exposure of the adult females to temperatures of 4°C, 37°C and 40°C resulted in distinct expression of heat shock protein 90 (HSP90). 40°C exposures led to a 4-fold increase in HSP90 expression compared to sandflies remaining at room temperature. Moreover, comparisons on the expression of HSP-coding genes between sandflies blood-fed with infected and non-infected meals showed a significant difference in profiles of HSP90, with females fed with uninfected meals having faster decreasing levels of HSP70 than females fed infected meals. The authors suggest the expression of certain heat shock proteins might be triggered to mitigate the thermal stress, when behavioural responses are otherwise not the most suitable option.

What I like about this preprint

I found the topic interesting, to better understand the relationship of pathogen vectors with their hosts. It is an interesting question being addressed.

Open questions

  1. Do you know if this response is conserved across other insect vectors?
  2. For other pathogens, the temperature at which the vectors live influences pathogen survival and development. Are your observations conserved across different Leishmania species?
  3. Did you see differences in parasite load in different compartments of the sandfly if sanflies remained at the same temperature throughout multiple days post-infected feed?
  4. What is the relevance of the activation of HSPs for parasite development?
  5. How does temperature ultimately impact L. mexicana transmission?

References

  1. Martins et al, Response to thermal and infection stresses in an American vector of visceral leishmaniasis, biorXiv, 2020.

 

Posted on: 21st December 2020

doi: https://doi.org/10.1242/prelights.26586

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