Abstract
Colonization resistance, i.e., the protective effects of associated microbiota for the animal host against pathogen infection, has been studied widely over the last 100 years. However, few molecules mediating colonization resistance have been identified. In the symbiosis formed by Delia antiqua and its associated microbes, six bacteria protect larvae from infection with the entomopathogen Beauveria bassiana, providing an ideal model to investigate the chemical mechanism for colonization resistance. Subsequently using this symbiotic system, we first compared effects of the six bacterial species, and one control bacterium (Klebsiella oxytoca) that showed no antifungal effects, on B. bassiana and its infection of D. antiqua Second, metabolomic profiles of the six bacteria and K. oxytoca were compared to identify candidate metabolites that may prevent infection. Third, the concentrations of candidate metabolites in situ from axenic and nonaxenic larvae were determined. Finally, effects of artificial metabolite cocktails on B. bassiana and its infection of D. antiqua larvae were determined. Results showed that compared to K. oxytoca, the six bacteria produced a metabolite cocktail showing inhibitory effects on conidial germination, mycelial growth of B. bassiana, and fungal infection. Our work revealed novel molecules that mediate colonization resistance, which could help in developing chemical mechanisms of colonization resistance. Moreover, this work may aid in discovery and expansion of new bioactive antibiotics, promoting development of prophylactic and therapeutic approaches for treating infectious diseases.IMPORTANCE The protection of associated microbiota for their animal hosts against pathogen infection has been studied widely over the last 100 years. However, how those microbes protect the animal host remains unclear. In former studies, body surface microbes of one insect, Delia antiqua, protected the insect larvae from infection with the entomopathogen Beauveria bassiana By comparing the metabolites produced by microbes that protect the insect and microbes that cannot protect the insect, the question of how the microbes protect the insect is answered. It turns out that body surface bacteria produce a metabolite cocktail that inhibits colonization of B. bassiana and consequently protects the insect. This work reveals novel molecules with antifungal activity, which may aid in discovery and expansion of new prophylactic and therapeutic natural chemicals for treating infectious diseases.
Highlights
Colonization resistance, i.e., the protective effects of associated microbiota for the animal host against pathogen infection, has been studied widely over the last 100 years
KaplanMeier analysis showed that the six bacterial strains including S. faecium B253, E. ludwigii B424 (Fig. S1b, 2 ϭ 0.942, df ϭ 1, P ϭ 0.334), S. plymuthica B585 (Fig. S1c, 2 ϭ 1.440, df ϭ 1, P ϭ 0.230), P. protegens B108 (Fig. S1d, 2 ϭ 0.875, df ϭ 1, P ϭ 0.350), C. freundii B505 (Fig. S1e, 2 ϭ 0.165, df ϭ 1, P ϭ 0.684), and S. maltophilia B263 (Fig. S1f, 2 ϭ 0.406, df ϭ 1, P ϭ 0.524) had no significant effects on the survival of axenic larvae compared to the control group
Survival rates of B. bassiana-treated axenic larvae inoculated with S. faecium B253, E. ludwigii B424, S. plymuthica B585, P. protegens B108, C. freundii B505, and S. maltophilia B263 were 67.5%, 64.1%, 66.7%, 82.1%, 89.7%, and 74.4%, respectively, and survival rates of B. bassiana-treated axenic larvae inoculated with of K. oxytoca B313 in each corresponding comparison were 15.0%, 12.5%, 17.5%, 17.5%, 32.4%, and 20.5%, respectively
Summary
Colonization resistance, i.e., the protective effects of associated microbiota for the animal host against pathogen infection, has been studied widely over the last 100 years. In the symbiosis formed by Delia antiqua and its associated microbes, six bacteria protect larvae from infection with the entomopathogen Beauveria bassiana, providing an ideal model to investigate the chemical mechanism for colonization resistance. Most studies have focused on symbioses of mammals and microbes, revealing the interaction between indigenous microbiota and migratory pathogens during the process of colonization resistance and even identifying various metabolites that mediate the process. These findings likely represent the tip of the iceberg, and such symbioses need further investigation. Due to insects’ worldwide distribution, rich diversity, the possibility of extrapolating research studies to vertebrates, and the relatively low cost of rearing, insect-microbe symbiotic systems have potential as alternative models to investigate and develop colonization resistance theory in broader taxonomic clades
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