Multiple lineages of Streptomyces produce antimicrobials within passalid beetle galleries across eastern North America

Abstract

Some insects form symbioses in which actinomycetes provide defense against pathogens by making antimicrobials. The range of chemical strategies employed across these associations, and how these strategies relate to insect lifestyle, remains underexplored. We assessed subsocial passalid beetles of the species Odontotaenius disjunctus, and their frass (fecal material), which is an important food resource within their galleries, as a model insect/actinomycete system. Through chemical and phylogenetic analyses, we found that O. disjunctus frass collected across eastern North America harbored multiple lineages of Streptomyces and diverse antimicrobials. Metabolites detected in frass displayed synergistic and antagonistic inhibition of a fungal entomopathogen, Metarhizium anisopliae, and multiple streptomycete isolates inhibited this pathogen when co-cultivated directly in frass. These findings support a model in which the lifestyle of O. disjunctus accommodates multiple Streptomyces lineages in their frass, resulting in a rich repertoire of antimicrobials that likely insulates their galleries against pathogenic invasion.

Microbiome assembly on Drosophila body surfaces benefits the flies to combat fungal infections

“…In addition, some insects (especially the social insects such as termites, ants, and honeybees) have evolved hygienic behaviors and social immunities to fight off fungal parasites ( Cremer, 2019 ; Heinze and Walter, 2010 ; Konrad et al., 2018 ; Ugelvig and Cremer, 2007 ). Otherwise, the assembly of Actinobacteria on the body surfaces of ants, beetles, and wasps has been demonstrated to the abilities to produce antifungal compounds to defend insects against fungal parasites ( Batey et al., 2020 ; Chevrette et al., 2019 ; Haeder et al., 2009 ; Kaltenpoth, 2009 ; Pessotti et al., 2021 ). Thus, insect external microbiotas may contribute to defense against fungal pathogens.…”

The power of poop: Defecation behaviors and social hygiene in insects

“…Given that termites and wood roaches are sister clades, this apparent defensive role of the fecal microbiome likely emerged in their common ancestor. Antimicrobial properties have also been discovered in earwig excrement [ 20 ] and passalid beetles ( Fig 1 ) [ 21 ], indicating that taxonomically widespread lineages of social insects have evolved similar strategies to inhibit pathogen growth. Antimicrobial effects of fecal microbiomes in social insects could be attributed to microbes colonizing the diet, surviving gut passage, and producing secondary metabolites in feces or those colonizing and selectively growing in feces.…”

“…The conditions within decaying wood potentially amplify the risk of pathogen breakouts and impose selective pressures for evolution of the fecal microbiome’s role in social immunity. The microbiological and chemical bases of feces-mediated defenses have been best dissected for actinobacteria in the subsocial wood-feeding beetle, Odontotaenius disjunctus , with similar roles suggested for strains isolated from guts of fungus-cultivating termites [ 21 , 26 ]. Feces-associated Actinomycetes collected from various populations of the beetle across the United States were observed to collectively produce a rich cocktail of antimicrobial metabolites from multiple families ( Fig 1 ) [ 21 ].…”

“…The microbiological and chemical bases of feces-mediated defenses have been best dissected for actinobacteria in the subsocial wood-feeding beetle, Odontotaenius disjunctus , with similar roles suggested for strains isolated from guts of fungus-cultivating termites [ 21 , 26 ]. Feces-associated Actinomycetes collected from various populations of the beetle across the United States were observed to collectively produce a rich cocktail of antimicrobial metabolites from multiple families ( Fig 1 ) [ 21 ]. In vitro inhibition assays with the isolated actinobacterial strains demonstrated a strong ability to inhibit M .…”

“…In vitro inhibition assays with the isolated actinobacterial strains demonstrated a strong ability to inhibit M . anisopliae [ 21 ].…”