Undetected: How germs circumvent the defenses of their ant hosts

Health is a constant race: pathogens want to gain the upper hand over the immune system and thus develop clever evasion strategies. The immune system tries to fight against it. One way to support the immune system of the affected person is medical intervention. However, this can also lead to undesirable adaptations in the pathogen, such as those seen in antibiotic-resistant bacteria. Another possible strategy is social intervention. Social groups such as ants try to fight infections with “social immunity”, i.e. h. with collective hygiene and health measures that prevent further spread of the disease in the community. Whether and how pathogens react to this type of group behavior is largely unknown.

The latest study by Professor Sylvia Cremer and her research team at the Institute of Science and Technology Austria (ISTA) presents the implications of this type of host-parasite interactions. Together with research colleagues at the University of Würzburg, the scientists took a closer look at ants. Their goal was to find out how pathogenic fungi respond to their hosts' social care during infection. The results, published today in Nature Ecology & Evolution, show: Fungi reduce their chemical recognition features to outwit their hosts' social immunity.

More spores but less cleaning

"Fungi infect the ants from the body surface and then continue to grow in the host body. However, the fungal spores are usually cleaned off by nest mates before they can even cause an internal infection," explains Barbara Milutinović, one of the lead authors, formerly a postdoc in the Cremer group and now a Marie Curie Sklodowska fellow at the Ruđer Bošković Institute in Croatia. In the experiments, the scientists examined Argentine ants (Linepithemahumile), which were infected with the pathogenic Metarhizium fungus and then kept either in the presence or absence of caring colony members. “In response to the care of the ant workers, the fungi have changed fundamentally,” continues Milutinović. Over ten infection cycles, those fungi that were cared for by nest mates increased their spore production compared to fungi that were only accompanied by individual ants. Sylvia Cremer adds: "The increased spore production helps the fungus to counteract social spore removal. What was surprising, however, was that the ants suddenly cleaned off fewer of the spores. This suggests that they no longer recognized the spores so easily."

Fungi lose their typical chemical profile

ISTA scientists worked with a chemical ecologist from the University of Würzburg to find out why the workers had problems identifying the fungi. Professor Thomas Schmitt there explains: "The fungi adapted to the social hosts showed a strong reduction in their membrane component ergosterol. Ergosterol is an essential building material of all fungi, and therefore makes it an identifying feature of fungi." If the ants were now exposed to pure ergosterol or a similar vertebrate analogue, it was shown that only the fungus-specific substance triggered intensive cleaning behavior in the ants. Milutinović summarizes: “Pathogens, in this case fungi, react to the presence of grooming ants by reducing characteristic signals – so they are no longer perceived as a threat and can thereby evade the social immunity of the colony.”

The results illustrate the influence that social hosts have on pathogens through their group behavior. "It is fascinating how collective hygiene measures trigger very specific evasion strategies in the pathogen. It would be exciting to see how the ants react in turn - perhaps by being able to detect ever lower levels of fungal signs," concludes Cremer.

Publication:

M. Stock, B. Milutinović, M. Hoenigsberger, A. V. Grasse, F. Wiesenhofer, N. Kampleitner, M. Narasimhan, T. Schmitt, S. Cremer. 2023. Pathogen evasion of social immunity. NatEcolEvol. DOI: 10.1038/s41559-023-01981-6

Project funding:

For this study, Sylvia Cremer received funding from the German Research Foundation (CR118/3-1) as part of the priority program SPP 1399 and the European Research Council (ERC) as part of the European Union's Horizon 2020 research and innovation program (No. 771402; EPIDEMICSonCHIP).

Information about animal testing:

The removal of the Argentine ant, a non-protected insect species, from the field was carried out in accordance with international regulations such as the Convention on Biological Diversity and the Nagoya Protocol on access to genetic resources and the fair and equitable sharing of the benefits arising from their use. All experimental work was carried out in accordance with European and Austrian law as well as institutional ethical guidelines.