Research Article: Endosymbiont-based immunity in Drosophila melanogaster against parasitic nematode infection

Date Published: February 21, 2018

Publisher: Public Library of Science

Author(s): Shruti Yadav, Joanna Frazer, Ashima Banga, Katherine Pruitt, Sneh Harsh, John Jaenike, Ioannis Eleftherianos, Wolfgang Arthofer.


Associations between endosymbiotic bacteria and their hosts represent a complex ecosystem within organisms ranging from humans to protozoa. Drosophila species are known to naturally harbor Wolbachia and Spiroplasma endosymbionts, which play a protective role against certain microbial infections. Here, we investigated whether the presence or absence of endosymbionts affects the immune response of Drosophila melanogaster larvae to infection by Steinernema carpocapsae nematodes carrying or lacking their mutualistic Gram-negative bacteria Xenorhabdus nematophila (symbiotic or axenic nematodes, respectively). We find that the presence of Wolbachia alone or together with Spiroplasma promotes the survival of larvae in response to infection with S. carpocapsae symbiotic nematodes, but not against axenic nematodes. We also find that Wolbachia numbers are reduced in Spiroplasma-free larvae infected with axenic compared to symbiotic nematodes, and they are also reduced in Spiroplasma-containing compared to Spiroplasma-free larvae infected with axenic nematodes. We further show that S. carpocapsae axenic nematode infection induces the Toll pathway in the absence of Wolbachia, and that symbiotic nematode infection leads to increased phenoloxidase activity in D. melanogaster larvae devoid of endosymbionts. Finally, infection with either type of nematode alters the metabolic status and the fat body lipid droplet size in D. melanogaster larvae containing only Wolbachia or both endosymbionts. Our results suggest an interaction between Wolbachia endosymbionts with the immune response of D. melanogaster against infection with the entomopathogenic nematodes S. carpocapsae. Results from this study indicate a complex interplay between insect hosts, endosymbiotic microbes and pathogenic organisms.

Partial Text

The soil dwelling nematode parasite Steinernema carpocapsae together with the Gram-negative bacteria Xenorhabdus nematophila form a mutualistic complex that is pathogenic to insects [1]. X. nematophila bacteria are localized in the gut of S. carpocapsae nematodes, which complete their life cycle in insect hosts [2]. The nematodes cause infections at the infective juvenile (IJ) stage, which is the developmentally arrested third larval stage analogous to the dauer stage of the non-pathogenic nematode, Caenorhabditis elegans [3]. Upon entry into the insect host, the nematodes release their bacteria into the hemolymph (insect blood), where the latter divide and produce a wide range of toxins and virulence factors that kill the host [4,5]. Although little is known about the contribution of nematode virulence factors to this process, we and others have shown that entomopathogenic (or insect pathogenic) nematodes lacking their mutualistic bacteria are still pathogenic to insects [6–10]. Recent studies have demonstrated that the nematodes produce certain molecules that suppress or promote evasion of certain insect immune responses allowing them to survive and reproduce in the insect host [11–13].

Previous studies in D. melanogaster adult flies have shown a protective role for Wolbachia, but not Spiroplasma, in response to certain viral infections [36,37], but not against bacterial infections [42,43,46,54]. Here, we explore the modulation of the D. melanogaster immune and metabolic responses, in the presence of Wolbachia alone or together with Spiroplasma, against S. carpocapsae nematodes. We find that the presence of Wolbachia alone or together with Spiroplasma in D. melanogaster larvae increases their survival upon infection with symbiotic S. carpocapsae; whereas the presence of both endosymbionts reduces larval survival in response to axenic worms. Interestingly, Drosophila neotestacea flies carrying Spiroplasma show delayed mortality when parasitized with Howardula aoronymphium nematodes; however, Wolbachia does not participate in the survival response to these nematodes [55,56]. Similarly, the presence of Wolbachia in Aedes pseudoscutellaris has no effect on the mosquito survival to Brugia pahangi filarial nematodes [57]. Our current results indicate that the effect of Wolbachia alone or together with Spiroplasma on S. carpocapsae during infection of D. melanogaster larvae depends on the presence or absence of the mutualistic X. nematophila bacteria in the nematode parasites.




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